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Everett  5!ranklin  Fnillips 

STRUCT1  D  DEVSLOmENT  OF 

''UND  EY^  OF  THE 
HONEY  BEE 


THE  LIBRARY 

OF 

THE  UNIVERSITY 

OF  CALIFORNIA 

DAVIS 


Structure    and    Development    of   the 

Compound    Eye    of  the 

Honey  Bee. 


BY  EVERETT  FRANKLIN  PHILLIPS,  PH.D., 

Harrison  Fellow  for  Research  in  Zoology, 
University  of  Pennsylvania. 


From  the  Proceedings  of  The  Academy  of  Natural  Science* 
of  Philadelphia,  February,  1905. 


I*sued  May  /,,  1905. 


UNIVERSITY  OF  CALIFORNIA 

LIBRARY 

DAVIS 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA. 


STRUCTURE  AND  DEVELOPMENT  OF  THE  COMPOUND  EYE  OF  THE 
HONEY  BEE. 

BY   EVERETT   FRANKLIN   PHILLIPS,    PH.D., 
Harrison  Fellow  for  Research  in  Zoology,  University  of  Pennsylvania. 

CONTENTS. 

I.     Introduction. 
II.     Methods. 

III.     Adult  Form  of  Eye  and  Ommatidium. 
[IV.     Embryology  and  Structure  in  Detail. 

1.  The  Entire  Eye. 

2.  Arrangement  of  Ommatidia. 

3.  Hair  Cells. 

V.     Retinular  Ganglion. 
VI.     The  Ommatidium. 

1.  Larva. 

2.  Pupa. 

a.  The  Retinula. 
6.  The  Cone  Cells. 

c.  The  Corneal  Pigment  Cells  and  the  Lens. 

d.  The  Outer  Pigment  Cells. 

3.  The  Adult  Ommatidium. 

a.  The  Retinula. 

VII.     Homologies  of  Component  Parts. 
VIII.     Summary. 
Literature. 
Explanation  of  Plates. 

I. — INTRODUCTION. 

The  morphology  of  the  compound  eye  has  puzzled  zoologists  for 
years,  and  much  work  has  been  done  on  the  subject,  but  so  diverse 
are  the  views  held  by  the  various  investigators  in  the  field  that  we  are 
far  from  a  final  solution  of  the  problem.  With  a  view  to  adding  some 
evidence  from  the  embryological  point  of  view  this  work  was  begun, 
in  the  belief  that  a  detailed  examination  of  this  one  insect  eye  would 
throw  some  light  on  the  adult  morphology. 

The  eye  of  the  common  honey  bee,  Apis  mellifera,  is  particularly 
favorable  for  embryological  work,  since  its  growth  is  gradual  and  the 
steps  of  development  well  marked  out.  The  material  is  also  easily 
obtained,  and  the  various  stages  of  growth  can  be  distinguished  by 
the  external  appearance  of  the  larvae  and  pupae.  It  is  also  favorable  for 
a  comparison  with  the  development  of  the  eye  of  Vespa,  which  was 
described  by  Patten,  since  it  is  desirable  to  find  how  far  his  results 
can  be  verified  on  a  closely  related  form.  The  large  number  of  omma- 


124  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

tidia  in  each  eye  make  the  preparation  of  sections  an  easier  matter, 
since  it  was  not  necessary  to  cut  so  many  eyes. 

The  adult  ommatidium  of  the  bee  was  briefly  described  and  figured 
by  Grcnachcr  in  his  celebrated  work,  Sehorgan  der  Arthropoden  (1879), 
and  has  been  figured  in  works  on  apiculture,  but  has  never  been  fully 
worked  out  in  the  adult  condition,  and  no  work  has  been  done  on  the 
development  of  the  eye.  Biitschli  (1860)  in  his  work  on  the  embryol- 
ogy of  the  bee  discusses  the  formation  of  the  eye,  but  does  not  go  into 
the  subject  of  the  development  of  the  ommatidium. 

This  work  was  taken  up  with  a  view  to  getting,  first  of  all,  a  complete 
description  of  the  development  and  structure,  and  in  addition  to  get 
some  light  on  certain  problems  which  are  of  especial  interest  from  a 
theoretical  standpoint.  The  innervation  of  the  ommatidium,  the 
method  of  formation  and  fundamental  plan  of  the  ommatidium,  the 
method  of  modification  of  numerical  plan  and  structure  in  the  evolu- 
tion, the  arrangement  of  ommatidia,  the  homology  of  various  cells 
in  different  ommatidia,  and  the  comparison  of  ommatidia  with  other 
sense-organs  are  questions  which  have  been  much  discussed,  and  in 
this  work  an  effort  has  been  made  to  apply  the  observations  made  to 
the  solution  of  these  problems.  This  is  done  not  without  the  realization 
that  some  of  these  things  can  be  settled  only  from  wide  comparisons, 
but  with  the  thought  that  a  piece  of  work  which  takes  in  the  whole 
course  of  development  is  of  more  value  than  superficial  observations 
of  a  large  number  of  forms.  Some  of  the  theories  are  merely  matters 
of  interpretation  rather  than  of  direct  observation,  and  must  remain 
so  until  decisive  observations  are  made,  but  in  matters  of  this  kind  the 
accumulation  of  evidence  is  of  decided  value. 

The  formation  of  the  optic  lobes  and  the  course  of  the  nervous  ele- 
ments through  them  are  problems  which  have  not  been  taken  up  for 
investigation  in  this  work.  Kenyon  has  worked  out  the  structure  of 
the  optic  lobes  for  Apis  in  detail  with  nerve  methods.  The  technique 
used  in  the  present  work  not  being  suitable  for  the  tracing  of  nerves, 
only  on  matters  concerning  the  nerve  endings  of  the  retinula  has  any 
investigation  been  made  in  this  work,  and  that  was  not  done  by 
Kenyon. 

In  the  matter  of  nomenclature  an  effort  has  been  made  to  avoid  the 
use  of  new  names  or  of  some  of  the  names  which  have  been  proposed 
by  some  workers  who  have  special  theories  to  uphold,  such  as  calyx, 
lentigen,  corneagen,  etc.  In  the  case  of  the  cells  which  surround  the 
cone-  I  have  used  the  name  corneal  pigment  cells,  since  they  have  a 
double  function.  In  other  cases  I  have  used  generally  accepted  names. 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  125 

The  plan  followed  in  this  paper  is  to  give,  first,  a  brief  description 
of  the  adult  eye,  so  that  further  discussion  will  be  more  intelligible, 
and  then  to  take  up  the  development  of  the  entire  eye  and  omma- 
tidium,  followed  by  a  detailed  description  of  the  adult  conditions, 
since  that  was  the  plan  followed  during  investigation,  and  is,  perhaps, 
the  order  which  will  be  most  clear  to  the  reader. 

This  work  was  taken  up  at  the  suggestion  of  Dr.  Thos.  H.  Mont- 
gomery, Jr.,  now  Professor  of  Zoology  in  the  University  of  Texas, 
and  was  completed  under  the  supervision  of  Professor  E.  G.  Conklin. 
To  both  I  am  indebted  for  many  valuable  suggestions  and  for  help 
throughout  the  work. 

II. — METHODS. 

Larvae  and  pupae  were  fixed  in  Flemming's  fluid,  Hermann's  fluid, 
picro-sulphuric,  picro-acetic  and  picric  acid  saturated  in  50  per  cent, 
alcohol,  but  of  these  the  Flemming  and  Hermann  preparations  yielded 
the  best  results.  For  the  smaller  larva?  it  was  not  necessary  to  dissect 
before  fixation,  but  for  older  larvae  and  pupae  the  head  was  removed 
to  make  penetration  easier.  For  adult  material,  where  penetration 
is  difficult,  the  best  fixative  was  acetic  acid,  generally  a  10  per  cent, 
or  20  per  cent,  acetic  solution  in  80  per  cent,  to  100  per  cent,  alcohol. 
Kleinenberg's  picro-sulphuric  and  picric  acid  in  50  per  cent,  alcohol 
were  also  used  with  fair  results  when  the  head  was  cut  in  two. 

The  material  was  all  cut  in  paraffine,  and  it  was  found  that  for  adult 
material  long  embedding  was  necessary,  four  to  eight  hours,  to  get  the 
paraffine  all  through  the  tissues.  Some  material  was  embedded  for  a 
shorter  time  to  see  whether  the  heat  had  produced  any  artifacts  in  the 
other  material  which  was  embedded  for  the  longer  period,  but  in  such 
cases  the  lens  invariably  separated  from  the  retinular  layer ;  no  differ- 
ence was  observed  in  the  internal  tissues  due  to  long  heating. 

In  staining,  the  best  results  were  obtained  in  the  use  of  Heidenhain's 
iron  hsematoxylin,  with  the  use  of  a  strong  mordant  for  a  long  time. 
For  material  of  this  kind  there  seems  to  be  no  better  stain.  It  was 
found  that  by  destaining  to  different  degrees  the  various  parts  of  the 
eye  would  show  differences  in  color,  the  rhabdome,  for  example,  stain- 
ing an  intense  black  in  rather  deeply  stained  material.  The  nerve 
fibrils  of  the  retinula  cells  also  stained  black  with  this  stain.  Other 
stains,  such  as  Delafield's  haematoxylin  and  eosine  or  Bordeaux  red, 
were  employed  with  very  good  results. 

For  depigmenting  Grenadier's  solution  with  a  somewhat  greater 
per  cent,  of  acid  was  used.  Parker's  solution  was  also  used,  though 
the  former  gave  the  better  results. 


128  PROCEEDINGS   OF   THE   ACADEMY   OF  [Feb.? 

ganglia.  During  the  larval  growth  the  eye  increases  greatly  in  size 
and  mitotic  figures  are  abundant,  the  mitosis  always  d  viding  the 
cells  lengthwise,  so  that  the  one-layered  condition  is  retained  until 
the  close  of  the  larval  period. 

During  the  semipupa  stage,  after  the  larva  is  sealed  up  by  the 
workers  of  the  hive  but  before  it  assumes  the  true  pupa  form,  the  one- 
layered  epithelium  gives  place  to  a  condition  in  which  all  the  cells  do 
not  extend  all  the  way  from  the  outer  surface  to  the  basement  mem- 
brane. This  is  brought  about  by  the  lengthening  of  some  cells,  the 
shortening  of  others  and  by  the  rearrangement  of  the  cells  in  a  manner 
to  be  described  later.  By  the  time  the  head  has  attained  the  size  and 
shape  of  the  adult,  the  cells  have  arranged  themselves  so  that  the 
ommatidia  are  completely  formed  and  no  more  mitoses  occur.  The 
development  of  the  ommatidia  from  now  on  consists  of  the  differentia- 
tion of  the  cell  elements  until  they  assume  their  adult  form.  The 
development  of  the  eye  as  a  whole  consists  of  a  thickening  of  the  organ 
and  the  laying  down  of  a  chitinous  lens  over  the  surface. 

At  the  sides  of  the  eye  of  the  young  pupa  the  appearance  is  as  shown 
in  text  fig.  2,  and  the  cells  which  correspond  to  the  cornea!  pigment 
cells  around  the  ommatidia  are  quite  numerous  and  shade  off  gradually 
into  the  cells  of  the  hypodermis  over  the  rest  of  the  head.  As  the  eye 
increases  in  thickness  by  the  lengthening  of  the  ommatidia  there  ap- 
pears a  dipping  in  of  the  cells  of  the  border,  so  that  there  is  an  invagi- 
nation  all  around  the  eye  where  the  secreting  surface  of  the  hypodermis 
is  pulled  down.  This  is  shown  by  a  thin  sheet  of  chitin  which  runs 
around  the  eye  (seen  in  section,  text  fig.  1)  in  the  late  pupa  and  adult 
eye.  This  chitin  is  similar  to  the  chitin  of  the  body  proper,  but  not 
like  that  over  the  eye.  This  imagination  must  not  be  confused  with 
such  an  invagination  as  is  described  by  Patten  for  the  formation  of  the 
lens  layer,  for  the  ommatidia  are  here  completely  formed  and  the  cor- 
neal  pigment  cells  have  moved  to  their  place  at  the  proximal  end  of 
the  cone  before  the  dipping  of  the  cells  here  described  takes  place. 

In  the  formation  of  the  optic  ganglia,  which  takes  place  by  the 
invagination  of  cells  of  the  hypodermis,  there  is  formed  a  brain  sheath 
— a  sheath  of  cells  covering  the  ganglia  and  still  continuous  with  the 
hypodermis  at  the  edge  of  the  eye.  This  layer  of  cells  runs  along 
proximal  to  the  basement  membrane  and  very  close  to  it  in  the  pupa 
stage.  As  the  retinular  ganglia  take  on  their  final  shape  these  cells 
are  pushed  away  from  the  basement  membrane,  and  are  seen  in  the 
adult  eye  as  strands  of  cytoplasm  woven  in  among  the  nerve  fibres 
between  the  basement  membrane  and  the  retinular  ganglion.  The 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  129 

nuclei  of  these  cells  are  smaller  and  are  easily  distinguishable  from  the 
retinular  ganglion  nuclei  which  lie  near  them  (see  text  fig.  3).  On 
the  edge  of  the  nerve  bundle  this  layer  is  continuous  with  the  brain 
sheath  in  the  adult.  The  strands  of  protoplasm  of  which  this  layer  of 
cells  is  composed  after  it  is  perforated  by  the  nerve  fibres  often  run 
up  close  to  the  basement  membrane  and  might  easily  be  mistaken  for 
nerve  fibres  to  the  outer  pigment  cells,  but  their  origin  indicates  that 
they  are  not  nerves  and  there  is  no  indication  of  any  nervous  connec- 
tion for  the  pigment  cells. 

Kenyon  recognized  this  layer  of  cells,  which  he  describes  as  follows  i1 
"The  outer  mass  (first  fibrillar  mass)  presents  a  lunar  appearance  in 
frontal  sections  (see  fig.  1  of  this  paper),  and  lies  close  inside  the  base- 
ment membrane  of  the  retina,  being  separated  from  it  by  sufficient 
space  for  the  entrance  of  large  tracheal  sacs  and  a  thin  layer  of  cells 
commingled  with  the  fibres  from  the  retina."  It  will  be  seen  that 
working  with  nerve  methods  this  author  did  not  recognize  them  as 
nerve  fibres,  nor  did  he  describe  any  nervous  connection  with  the  pig- 
ment cells.  Frequently  these  strands  of  protoplasm  run  close  to  the 
basement  membrane  and  there  spread  out  as  a  pyramidal  protoplasmic 
mass  lying  between  the  nerve  fibrils.  This  is  particularly  noticeable 
in  pupa  stages  before  this  layer  of  cells  is  so  greatly  distorted. 

The  basement  membrane  is  made  up  of  a  fusion  of  the  proximal 
ends  of  the  outer  pigment  cells  with  the  pigmented  portion  of  the  reti- 
nular cells.  This  makes  a  sheet  of  cytoplasm,  perforated  where  the 
nerve  fibres  pass  from  the  retinular  cells,  which  can  easily  be  macerated 
away  from  the  other  elements  of  the  eye  and  is  easily  distinguishable 
on  account  of  its  deeply  pigmented  condition.  The  nerve  fibres  from 
the  retina  pass  through  this  and  are  seen  as  more  or  less  separated  on 
a  section  through  that  region  (fig.  18).  This  basement  membrane  is 
continuous  with  the  basement  membrane  of  the  hypodermal  cells. 
Fig.  10  shows  diagrammatically  the  structure  of  the  base  of  an^omma- 
tidium  and  the  elements  which  compose  the  basement  membrane,'  but 
does  not  show  the  separation  of  nerve  fibrils,  since  that  is  seen  clearly 
only  in  cross  sections  through  that  region. 

There  are  no  trachese  distal  to  the  basement  membrane  in  the  com- 
pound eye  of  the  bee  such  as  have  been  described  in  other  eyes,  espe- 
cially among  the  Diptera.  Exception  must  be  taken  to  the  statement 
of  Hickson2  that  "no  spirally-marked  trachese  penetrate  the  optic  tract 
at  any  part  of  its  course  in  Hymenoptera."  Between  the  basement 

1  P.  369. 

2  P.  223. 


130 


PROCEEDINGS  OF  THE  ACADEMY  OF 


[Feb., 


ret.gang.rj. 


Fig.  3. — Section  below  basement  mem- 
brane, showing  retinular  ganglion  cells 
and  nerve  fibrils  from  ommatidia. 


membrane  and  the  retinular  ganglion  tracheae  with  spiral  markings 
occur  in  all  specimens  examined  (see  text  fig.  3),  but  the  statement  of 

Hickson  holds  good  for  all  other 
parts  of  the  optic  tract  as  far 
as  has  been  observed.  Kenyon 
also  mentions  the  presence  of 
tracheae  in  this  region. 


2.  Arrangement  of  Ommatidia. 


The  facets  of  the  lens  are 
arranged  in  hexagons,  as  is  true 
for  so  many  insect  eyes,  but  this 
is  probably  not  a  primitive  con- 
dition. Hexagonal  arrangement 
is  what  is  produced  whenever 
any  circular  objects  are  closely 

pressed  together,  just  as  the  cells  of  the  honeycomb  are  hexagonal, 
and  this  undoubtedly  explains  the  shape  and  arrangement  of  the 
facets.  Parker  (for  Crustacea)  looks  upon  unfaceted  eyes  as  primi- 
tive, and  probably  this  is  true  for  insects  also.  We  have,  however, 
in  the  proximal  portion  of  the  eye  a  different  arrangement  which 
is  perhaps  more  primitive  than  the  hexagonal  method.  At  any 
level  proximal  to  the  cone  cells  the  ommatidia  are  arranged  in  parallel 
rows,  and  the  nearer  we  come  to  the  base  of  the  ommatidia  the 
clearer  is  this  arrangement,  until  on  a  section  at  the  level  of  the  base- 
ment membrane  (fig.  18)  we  see  this  parallel  arrangement  very 
marked.  Since  here  we  get  a  condition  in  which  the  ommatidia  are 
not  pressed  together  and  therefore  are  not  modified  mechanically, 
it  probably  represents  a  more  primitive  condition  than  that  found 
in  the  lens  region.  In  the  pupa,  even  the  facets  do  not  have  as  marked 
a  hexagonal  arrangement  as  they  have  later,  and  in  the  larva  we  get 
an  arrangement  identical  with  that  of  the  bases  of  the  adult  ommatidia. 
The  numerical  plan  and  shape  of  the  parts  of  the  ommatidium  may 
have  something  to  do  with  the  arrangement.  The  retinular  cells  are 
eight  in  number,  but  four  of  these  are  wider  than  those  which  alternate 
with  them,  and  as  a  result  a  cross-section  of  the  retina  is  roughly  a 
square.  The  outer  pigment  cells  are  twelve  in  number  when  thfir 
arrangement  is  unmodified  by  hair  cells,  and  this  number  readily  ar- 
ranges itself  into  a  square  with  three  on  a  side,  or  into  a  hexagon  with 
two  on  a  side.  Since  the  outer  pigment  cells  are  simply  strands  of 
cytoplasm  they  readily  accommodate  themselves  to  any  change  of 


1905.]  NATURAL   SCIENCES   OF    PHILADELPHIA.  131 

arrangement  and  are  not,  as  a  rule,  without  some  bend,  so  these  cells 
could  scarcely  modify  an  ommatidial  plan  of  arrangement.  The  base- 
ment membrane  is  considerably  smaller  in  area  than  the  lens  chitin, 
and  as  a  result  the  room  provided  for  each  ommatidium  is  considerably 
decreased,  so  that  in  contrast  with  what  has  been  stated,  that  the 
ommatidia  are  not  so  crowded  proximal  to  the  cone,  it  might  be  sup- 
posed that  the  converse  would  be  true.  However,  the  fact  is  that  in 
cross-section  a  larger  proportion  of  space  is  occupied  by  outer  pigment 
cells,  the  interommatidial  spaces,  near  the  base  of  the  ommatidia  than 
near  the  lens;  and  since,  as  above  stated,  these  cells  are  flexible  and 
not  crowded,  it  scarcely  seems  to  follow  that  this  parallel  arrangement 
is  due  to  crowding. 

The  hexagonal  arrangement  is  undoubtedly  the  common  plan,  at 
least  as  far  as  the  lens  is  concerned,  and  the  tetragonal  arrangement 
may  be  derived  from  it  as  held  by  Parker,  and  his  arguments  for  such 
an  origin  seem  good ;  but,  on  the  other  hand,  the  hexagonal  arrangement 
could  scarcely  give  rise  to  the  tetragonal  unless  preceding  the  hex- 
agonal facets  the  ommatidia  were  in  squares,  so  that  the  secondary 
crowding  would  bring  about  the  primitive  arrangement  again.  Taking 
again  the  case  of  the  honeycomb,  no  additional  crowding  could  possibly 
make  the  cells  square,  for  the  more  the  circular  walls  (the  primitive 
cells)  are  crowded  the  more  truly  they  become  hexagonal.  However, 
if  the  walls  were  made  of  four  parts,  as  is  the  cone,  and  if  they  were 
fastened  at  their  bases  in  parallel  rows,  then  additional  crowding  might 
cause  the  lens  to  lose  its  circular  outline  and  become  square,  in  which 
case  the  hexagonal  arrangement  of  the  lens  would  be  lost.  It  seems 
probable  that  the  cone  determines  the  arrangement  rather  than  the 
lens-secreting  cells,  and  Parker's  figures  of  Gonodactylus  (Parker,  1890, 
PI.  VIII,  fig.  93),  in  which  the  tetragonal  arrangement  is  found  in  the 
large  ommatidia  and  not  in  the  small  ones,  lend  support  to  this  view. 

To  sum  up,  it  seems  probable  that  the  arrangement  of  ommatidia, 
where  they  are  sufficient  in  number  to  be  said  to  have  any  plan  at  all, 
is  normally  the  tetragonal  plan.  If  the  cones  are  somewhat  com- 
pressed, as  they  generally  are  on  account  of  the  way  in  which  a  com- 
pound eye  is  made  up,  a  hexagonal  arrangement  of  the  distal  parts  of 
the  ommatidia  results;  but  if  the  pressure  is  sufficient  to  cause  the 
cone  to  lose  its  circular  form  then  it  becomes  a  square,  and  the  facet 
plan  again  becomes  tetragonal. 

3.  Hair  Cells. 

The  entire  lens  of  the  eye  of  the  bee,  especially  in  the  younger 
individuals,  is  covered  with  large  hairs,  unlike  those  of  the  rest  of 


132 


PROCEEDINGS  OF  THE  ACADEMY  OF 


[Feb., 


the  body  in  being  unbranched.  These  hairs  are  secreted  by  large 
hair-mother  cells  which  lie  among  the  outer  pigment  cells  between 
the  ommatidia,  and  their  development  is  of  interest  on  account 


Fig.  4. — a.  Hair  cell  of  young  pupa,  showing  three  nuclei  and  intracellular 
duct.  b.  Cross-section  through  pupal  retinulse,  showing  one  hair  cell.  c.  Cross- 
section  through  hair  just  at  level  of  cones,  showing  structure  of  intracellular 
duct.  d.  Cross-section  distal  to  c  and  beyond  surface  of  eye.  e.  Older  pupa 
hair  cell.  /.  Hair  cell  of  adult,  showing  relation  to  cone  and  lens. 

of  the  presence  in  them  of  an  intracellular  duct  and  because  of  their 
binucleated  condition.  In  the  larval  eye  these  hair  cells  cannot  be 
definitely  located,  but  there  are  certain  large  cells  with  peculiar  nuclei 


1905.]  NATURAL   SCIENCES    OF   PHILADELPHIA.  133 

which  are  probably  hair  cells.  In  the  early  pupa  these  cells  are  large 
and  have  two,  or  sometimes  three,  nuclei,  but  when  a  third  nucleus  is 
present  it  is  considerably  smaller  than  the  two  more  distally  placed 
ones.  In  the  early  stages  this  polynucleated  cell  contains  an  intra- 
cellular  duct  which  opens  into  the  tubular  hair,  and  through  this  duct 
passes  the  secretion  products  of  the  cell  for  the  formation  of  the  hair. 
The  hair  proper  is  tubular  and  in  material  stained  in  iron  hsematoxylin 
darker  lines  appear  in  the  walls,  and  these  structures  extend  for  a  short 
distance  down  into  the  cell  proper  around  the  duct.  The  duct  has 
well-marked  boundaries,  docs  not  branch,  and  generally  coils  around 
the  second  nucleus  (text  fig.  4). 

As  the  lens  increases  in  thickness  the  hairs  elongate  by  the  secretion 
of  the  hair  cells,  and  as  this  goes  on  the  cytoplasm  of  the  cell  is  used 
up,  until  finally,  in  the  adult  eye,  the  cell  has  about  one-sixth  the 
volume  it  had  in  the  early  pupal  eye.  In  the  intracellular  duct  and 
in  the  hair  duct  the  products  of  secretion  may  be  observed  in  fixed 
material  as  darker  bodies  of  irregular  shape. 

These  hairs  and  hair  cells  have  no  nerve  connection,  as  far  as  I  can 
observe,  and  are  therefore  not  sensoiy  hairs.  Just  why  the  entire  eye 
should  be  covered  by  hairs  is  hard  to  explain,  for  they  must  undoubted- 
ly obscure  vision,  and  since  such  a  hindrance  is  present  we  should 
expect  to  find  it  compensated  for  by  some  sensory  function  on  the  part 
of  the  hair.  I  can  find  no  indication  that  such  is  the  case.  It  is  worthy 
of  note  that  the  older  bees  have  lost  most  of  the  hairs  both  on  the  eyes 
and  on  the  body  by  the  time  they  need  the  eyes  for  prolonged  flight. 
The  younger  bees,  up  to  nearly  three  weeks  of  age,  leave  the  hive  but 
rarely,  and  then  for  short  distances  only,  but  the  older  bees  which  take 
long  journeys  have  the  eyes  much  more  bare.  It  is  also  noticeable 
that  all  the  bees,  but  especially  the  drones,  brush  the  hairs  so  that  they 
all  point  down  toward  the  mouth  just  before  leaving  the  hive  entrance. 
No  doubt,  in  the  hive,  the  head,  which  is  so  frequently  put  into  the 
cells,  becomes  soiled  with  honey  and  pollen,  and  this  action  of  brushing 
may  be  merely  to  remove  dirt:  but,  on  the  other  hand,  the  arranging 
of  the  partly  transparent  hairs  in  one  direction  may  produce  certain 
results  of  refraction  which  are  favorable. 

In  Vanessa,  Johansen  describes  hair  cells  as  running  the  length  of 
the  ommatidia  without  an  intracellular  duct  and  with  but  one  nucleus. 
He  is  able  to  locate  these  cells  at  an  earlier  stage  than  has  been  pbssible 
for  the  bee  on  account  of  the  proximal  position  of  the  nucleus.  From 
the  figure  of  a  cross-section  of  the  cornea  it  would  appear  that  these 
cells  are  not  so  abundant  as  in  Apis.  Patten  figures  hair  cells  .for 


134  PROCEEDINGS   OF   THE   ACADEMY    OF  [Feb., 

Vespa  very  similar  to  those  here  described,  but  I  am  unable  to  find 
the  nerve  connections  which  he  describes.  Semper  and  Breitenbach 
also  describe  such  hair  cells  for  Lepidoptera. 

The  number  of  facets  in  the  different  kinds  of  individuals  of  the  col- 
ony differs  considerably.  The  drones  (males)  have  an  extremely 
large  number  of  ommatidia,  the  eyes  meeting  on  the  top  of  the  head, 
and  as  a  result  the  three  ocelli  are  crowded  down  to  the  front  of  the 
head.  The  workers  and  queens  have  a  considerably  smaller  number, 
about  one-third  as  many,  and  the  ocelli  are  located  at  the  top  of  the 
head.  It  is  not  clear  why  the  drones  should  have  a  larger  number  of 
ommatidia  than  the  females  of  the  colony,  since  they  do  not  seem  to 
need  so  much  larger  range  of  vision.  The  only  reason  which  might 
be'suggested  from  a  knowledge  of  the  habits  of  the  two  sexes  is  that 
at  the  time  when  the  queen  takes  her  "mating  flight"  she  flies  almost 
directly  upward,  after  a  preliminary  circle  or  two  near  the  hive,  and 
then  often  flies  to  some  distance  from  the  hive ;  this  manner  of  flying 
making  more  probable  a  mating  with  a  drone  from  some  other  colony 
than' her" own.  Drones  do  not,  as  a  rule,  fly  as  high  as  does  the  queen, 
and  it  would  be  advantageous  to  have  the  eyes  extending  to  the  top 
of  the  head  in  order  to  follow  the  queen's  flight.  As  soon  as  a  queen 
starts  upward  any  drones  which  are  flying  near  at  hand  start  upward 
after  her,  the  eyes  on  the  top  of  the  head  making  it  possible  for  them 
to  see  her. 

To  say  that  this  difference  has  arisen  on  this  account  scarcely  seems 
justifiable,  for  it  would  seem  easier  for  natural  selection,  sexual  selec- 
tion, or  whatever  other  factor  is  potent  here,  to  modify  the  habits  of 
flight  rather  than  to  enlarge  an  organ  so  much  as  in  this  case.  This 
much  may,  however,  be  said  with  a  good  deal  of  surety:  two  things 
which  would  be  likely  to  be  acted  on  by  selection  in  the  bee  are  acute- 
ness  and  range  of  vision  and  the  power  of  flight. 

V. — RETINULAR  GANGLION. 

In  the  early  larval  stages  the  optic  ganglia  are  clearly  marked  out, 
but  the  retinular  ganglia  are  not.  The  only  indication  of  the  retinular 
ganglia  is  a  number  of  cells  which  lie  near  the  basement  membrane  of 
the  eye,  principally  at  the  posterior  margin.  During  the  larval  growth 
the  nerve  fibres  from  the  ommatidia  grow  in  from  the  retinular  cells, 
and  as  this  growth  goes  on  the  cells  of  what  are  to  be  the  retinular 
ganglia  are  pushed  farther  away  from  the  basement  membrane  and 
assume  their  more  definite  position.  Finally,  in  the  adult  animal  the 


1905.]  NATURAL    SCIENCES    OF    PHILADELPHIA.  135 

nerve  fibres  from  the  ommatidia  form  a  relatively  compact  mass  and 
the  retinular  ganglion  cells  are  scattered  through  the  fibres  in  such  a 
way  as  to  have  the  appearance  of  a  definite  ganglion.  The  nuclei  of 
the  retinular  ganglion  are  no  longer  nearly  in  one  plane,  but  are  scat- 
tered for  a  considerable  distance  between  the  basement  membrane 
and  the  outer  fibrillar  mass  due  to  the  crowding  of  the  nerve  fibres. 

The  question  naturally  arises  as  to  the  number  of  cells  of  the  retinular 
ganglion  as  compared  with  the  number  of  ommatidia.  A  count  is, 
of  course,  impossible,  but  careful  examination  reveals  that  there  can- 
not be  many  more  than  one  to  an  ommatidium,  certainly  not  one  to 
each  retinular  cell.  The  eight  nerve  fibres  from  each  group  of  retinular 
cells  are  entirely  separate,  but  lie  close  together,  so  that  probably  one 
and  only  one  retinular  ganglion  cell  receives  the  impulse  carried  from 
the  retina  on  eight  nerve  processes,  and  consecutive  cross-sections  indi- 
cate that  the  eight  nerve  fibrils  surround  the  thick  part  of  the  retinular 
ganglion  cell  where  the  nucleus  is  located  and  transmit  the  impulse  by 
contact. 

In  his  description  of  this  region  Kenyon  says:3  "The  elements 
from  the  retina  terminate  each  in  a  small  tuft  of  fine  branches  in  the 
outer  fibrillar  body,  and  come  in  contact  with  the  fine  lateral  branchlets 
given  off  in  the  same  region  by  fibres  originating  from  the  cells  of  Ber- 
ger's  granular  layer  (retinular  ganglion)."  The  tuft  of  fine  branches 
here  mentioned  are  the  separate  nerve  fibres  from  the  retinulse.  I  have 
been  unable  to  see  the  fine  branches  of  the  retinular  ganglion  cells. 

The  retinular  ganglion  cell  in  turn  sends  in  its  fibre  through  the  first 
fibrillar  mass,  and  then  through  the  outer  chiasma  to  the  opposite 
side  of  the  group  of  ganglia,  where  the  impulse  is  given  over  to  a  cell 
of  the  first  optic  ganglion.  From  here  on  the  tracing  of  the  fibres 
requires  special  nerve  methods  which  were  not  employed  in  this  work. 
However,  this  much  is  evident :  the  cells  of  the  first  optic  ganglion  send 
their  fibres  through  the  second  fibrillar  mass  and  through  the  inner 
chiasma  to  the  second  optic  ganglion,  where  the  impulse  is  probably 
again  transferred  to  another  cell  which,  in  turn,  carries  it  to  the  brain. 
The  course  of  these  fibres  has  been  worked  out  in  detail  by  Kenyon 
(1897),  and  in  my  work  I  find  nothing  to  contradict  his  results,  although 
the  methods  used  in  my  work  were  not  such  as  to  warrant  either  a 
positive  denial  or  confirmation  of  his  work. 

»P.  374. 


134  PROCEEDINGS   OF   THE   ACADEMY    OF  [Feb., 

Vespa  very  simDar  to  those  here  described,  but  I  am  unable  to  find 
the  nerve  connections  which  he  describes.  Semper  and  Breitenbach 
also  describe  such  hair  cells  for  Lepidoptera. 

The  number  of  facets  in  the  different  kinds  of  individuals  of  the  col- 
ony differs  considerably.  The  drones  (males)  have  an  extremely 
large  number  of  ommatidia,  the  eyes  meeting  on  the  top  of  the  head, 
and  as  a  result  the  three  ocelli  are  crowded  down  to  the  front  of  the 
head.  The  workers  and  queens  have  a  considerably  smaller  number, 
about  one-third  as  many,  and  the  ocelli  are  located  at  the  top  of  the 
head.  It  is  not  clear  why  the  drones  should  have  a  larger  number  of 
ommatidia  than  the  females  of  the  colony,  since  they  do  not  seem  to 
need  so  much  larger  range  of  vision.  The  only  reason  which  might 
be'suggested  from  a  knowledge  of  the  habits  of  the  two  sexes  is  that 
at  the  time  when  the  queen  takes  her  "mating  flight"  she  flies  almost 
directly  upward,  after  a  preliminary  circle  or  two  near  the  hive,  and 
then  often  flies  to  some  distance  from  the  hive ;  this  manner  of  flying 
making  more  probable  a  mating  with  a  drone  from  some  other  colony 
than'her'own.  Drones  do  not,  as  a  rule,  fly  as  high  as  does  the  queen, 
and  it  would  be  advantageous  to  have  the  eyes  extending  to  the  top 
of  the  head  in  order  to  follow  the  queen's  flight.  As  soon  as  a  queen 
starts  upward  any  drones  which  are  flying  near  at  hand  start  upward 
after  her,  the  eyes  on  the  top  of  the  head  making  it  possible  for  them 
to  see  her. 

To  say  that  this  difference  has  arisen  on  this  account  scarcely  seems 
justifiable,  for  it  would  seem  easier  for  natural  selection,  sexual  selec- 
tion, or  whatever  other  factor  is  potent  here,  to  modify  the  habits  of 
flight  rather  than  to  enlarge  an  organ  so  much  as  in  this  case.  This 
much  may,  however,  be  said  with  a  good  deal  of  surety:  two  things 
which  would  be  likely  to  be  acted  on  by  selection  in  the  bee  are  acute- 
ness  and  range  of  vision  and  the  power  of  flight. 

V. — RETINULAR  GANGLION. 

In  the  early  larval  stages  the  optic  ganglia  are  clearly  marked  out, 
but  the  retinular  ganglia  are  not.  The  only  indication  of  the  retinular 
ganglia  is  a  number  of  cells  which  lie  near  the  basement  membrane  of 
the  eye,  principally  at  the  posterior  margin.  During  the  larval  growth 
the  nerve  fibres  from  the  ommatidia  grow  in  from  the  retinular  cells, 
and  as  this  growth  goes  on  the  cells  of  what  are  to  be  the  retinular 
ganglia  are  pushed  farther  away  from  the  basement  membrane  and 
assume  their  more  definite  position.  Finally,  in  the  adult  animal  the 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  135 

nerve  fibres  from  the  ommatidia  form  a  relatively  compact  mass  and 
the  retinular  ganglion  cells  are  scattered  through  the  fibres  in  such  a 
way  as  to  have  the  appearance  of  a  definite  ganglion.  The  nuclei  of 
the  retinular  ganglion  are  no  longer  nearly  in  one  plane,  but  are  scat- 
tered for  a  considerable  distance  between  the  basement  membrane 
and  the  outer  fibrillar  mass  due  to  the  crowding  of  the  nerve  fibres. 

The  question  naturally  arises  as  to  the  number  of  cells  of  the  retinular 
ganglion  as  compared  with  the  number  of  ommatidia.  A  count  is, 
of  course,  impossible,  but  careful  examination  reveals  that  there  can- 
not be  many  more  than  one  to  an  ommatidium,  certainly  not  one  to 
each  retinular  cell.  The  eight  nerve  fibres  from  each  group  of  retinular 
cells  are  entirely  separate,  but  lie  close  together,  so  that  probably  one 
and  only  one  retinular  ganglion  cell  receives  the  impulse  carried  from 
the  retina  on  eight  nerve  processes,  and  consecutive  cross-sections  indi- 
cate that  the  eight  nerve  fibrils  surround  the  thick  part  of  the  retinular 
ganglion  cell  where  the  nucleus  is  located  and  transmit  the  impulse  by 
contact. 

In  his  description  of  this  region  Kenyon  says:3  "The  elements 
from  the  retina  terminate  each  in  a  small  tuft  of  fine  branches  in  the 
outer  fibrillar  body,  and  come  in  contact  with  the  fine  lateral  branchlets 
given  off  in  the  same  region  by  fibres  originating  from  the  cells  of  Ber- 
ger's  granular  layer  (retinular  ganglion)."  The  tuft  of  fine  branches 
here  mentioned  are  the  separate  nerve  fibres  from  the  retinulse.  I  have 
been  unable  to  see  the  fine  branches  of  the  retinular  ganglion  cells. 

The  retinular  ganglion  cell  in  turn  sends  in  its  fibre  through  the  first 
fibrillar  mass,  and  then  through  the  outer  chiasma  to  the  opposite 
side  of  the  group  of  ganglia,  where  the  impulse  is  given  over  to  a  cell 
of  the  first  optic  ganglion.  From  here  on  the  tracing  of  the  fibres 
requires  special  nerve  methods  which  were  not  employed  in  this  work. 
However,  this  much  is  evident :  the  cells  of  the  first  optic  ganglion  send 
their  fibres  through  the  second  fibrillar  mass  and  through  the  inner 
chiasma  to  the  second  optic  ganglion,  where  the  impulse  is  probably 
again  transferred  to  another  cell  which,  in  turn,  carries  it  to  the  brain. 
The  course  of  these  fibres  has  been  worked  out  in  detail  by  Kenyon 
(1897),  and  in  my  work  I  find  nothing  to  contradict  his  results,  although 
the  methods  used  in  my  work  were  not  such  as  to  warrant  either  a 
positive  denial  or  confirmation  of  his  work. 

8  P.  374. 


gi     PROCEEDINGS    OF    THE    ACADEMY    OF 


[Feb., 


VI. — THE  OMMATIDIUM. 
1.  The  Larva. 

In  the  larva,  justTafter  being  hatched  from  the  egg,  I  have  been 
unable  to  find  any  indication  of  the  grouping  of  cells  which  are  later  to 
go  together  to  form  a  single  ommatidium.  The  eye  at  this  time  is  a 
simple  layer  of  the  thickened  hypodermis  with  the  nuclei  arranged  one 
above  the  other.  At  this  time,  and  throughout  the  entire  larval  period, 
mitotic  figures  are  abundant,  the  spindles  always  having  then"  axes 
at  right  angles  to  the  length  of  the  cell  and  dividing  the  cells  lengthwise. 


Fig.  5.-^-a.  Longitudinal  section  of  larval  ommatidia.  b. 
Cross-section  near  surface  of  eye,  showing  first  differentiation 
of  rhabdome  (rhb.)  as  a  clear  space  in  the  retinula  (ret.),  c. 
Cross-section  at  a  lower  level,  d.  Cross-section  of  a  very  young 
larva,  each  division  line  representing  a  complete  ommatidium. 

The  division  figures  seem  to  be  more  abundant  near  the  outer  surface 
of  the  epithelium. 

About  one  day  after  leaving  the  egg,  when  the  larva  has  about 
doubled  in  size,  a  tangental  section  of  the  eye  at  right  angles  to  the 
long  axes  of  the  cells  at  the  outer  surface  reveals  a  grouping  of  cells 
as  represented  in  text  fig.  5d.  The  lines  in  this  figure  do  not  represent 
cell  boundaries  but  are  the  boundaries  of  groups  of  cells ;  each  group 
contains  four  or  five  cells  at  this  time,  the  nuclei  of  these  cells  being 
directly  one  above  the  other.  The  cell  groups  are  tetragonal  and  are 
arranged  roughly  in  parallel  rows.  In  longitudinal  section  these  groups 
appear  as  made  up  of  long  strands  with  superimposed  nuclei  about  the 
diameter  of  the  entire  width  of  the  group  of  cells.  That  these  are  the 
beginnings  of  the  ommatidia  is  evident  since  they  can  be  traced  through 


1905.]  NATURAL   SCIENCES    OF    PHILADELPHIA.  137 

all  the  larval  stages  to  the  pupa,  where  the  ommatidia  are  definitely 
marked.  This  is  further  indicated  by  the  fact  that  they  are  arranged 
in  the  same  way  as  are  the  proximal  ends  of  the  ommitidia,  even  in 
the  adult  eye.  It  should  be  borne  in  mind  that  this  epithelium  is 
strictly  one-layered,  and  this  is  true  all  through  the  larval  period. 

During  the  larval  period,  as  above  stated,  mitotic  figures  are  abun- 
dant, and  as  a  result  of  these  divisions  the  groups  come  to  be  composed 
of  more  and  more  cells,  but  it  is  not  until  a  late  larval  period  (about 
four  and  a  half  days  from  the  hatching  of  the  egg  for  worker  larvae) 
that  any  further  differentiation  is  observable,  except  possibly  that  the 
nuclei  of  some  of  the  cells  are  larger  than  others  in  the  same  group. 
At  this  late  larval  period  the  cells  arrange  themselves  as  a  spindle- 
shaped  mass  surrounded  by  smaller  cells  whose  smaller  nuclei  lie  in 
the  space  left  at  the  outer  end  of  the  spindle.  Mitotic  figures  are  now 
absent  except  an  occasional  one  in  the  smaller  cells,  but  so  far  none 
have  been  observed  in  the  larger  centrally  placed  cells  of  the  group. 
The  number  of  cells  in  the  spindle  is  hard  to  determine,  since  the 
nuclei  are  at  different  levels  and  the  cell  boundaries  are  not  visible. 
All  the  nuclei  of  the  central  bundle  of  cells  are  some  distance  below  the 
surface.  There  are  certainly,  however,  not  more  than  eight  or  nine,  the 
number  of  retinular  cells  of  the  adult  ommatidium.  At  the  distal 
end  of  this  spindle  a  differentiation  of  cytoplasm  takes  place,  and  a 
clear  space  is  formed  in  the  centre  of  the  cells  in  the  very  granular 
protoplasm,  and  this  I  believe  to  be  the  beginning  of  the  rhabdome. 
A  cross-section  near  the  outer  surface  of  the  cell  mass  shows  this  clear 
space  surrounded  by  granular  cytoplasm  of  the  spindle  cells,  and  this 
in  turn  surrounded  by  nuclei  arranged  around  the  central  bundle. 
These  outer  nuclei  are  not  as  yet  differentiated,  so  that  their  future 
fate  cannot  be  determined.  The  cells  of  the  spindle  by  this  time  have 
sent  out  protoplasmic  processes  toward  the  optic  lobes  which  become 
the  nerve  fibres  of  the  ommatidium,  so  that  at  any  rate  some  of  the 
spindle  becomes  the  retinula. 

Several  facts  seem  to  indicate  that  the  spindle-shaped  centre  of  the 
ommatidium  goes  to  form  only  the  retinula:  (1)  There  are  no  nuclei 
near  the  outer  surface,  as  one  wrould  expect  were  crystalline  cone  cells 
to  be  formed  from  any  of  the  cells ;  (2)  there  are  not  enough  cells  to 
form  both  retinula  and  crystalline  cone  cells,  and  since  no  mitotic 
figures  have  been  observed  they  have  undoubtedly  ceased  division; 
(3)  a  clear  space  is  formed  at  the  distal  end  of  the  spindle  by  a  differen- 
tiation of  the  cytoplasm,  possibly  the  beginning  of  the  rhabdome,  since 
it  is  in  this  portion  of  the  retinula  that  the  rhabdome  is  seen  in  the 


138  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

youngest  pupal  eye  observed  (just  after  the  semipupa  stage).  The 
number  of  nuclei  around  the  spindle  throws  no  light  on  this,  since  they 
are  still  dividing  occasionally  and  their  number  in  the  adult  is  not 
fixed. 

Considerable  stress  has  been  laid  on  the  fate  of  this  spindle-shaped 
mass  of  cells,  since  the  determination  of  this  fact  alone  is  of  such  great 
importance  in  the  consideration  of  the  morphology  of  the  ommatidium. 
That  the  outer  pigment  cells  are  morphologically  peripheral  to  the 
crystalline  cone  and  rctinula  no  one  would  deny.  The  position  of  the 
corneal  pigment  cells  might  be  a  doubtful  point  if  they  were  derived 
from  a  separate  layer  of  cells  formed  by  invagination  of  the  entire  eye, 
but  as  no  such  invagination  occurs  in  the  bee,  and  as  at  an  early  pupa 
stage  they  are  clearly  outside  the  cone,  I  think  there  can  be  no  doubt 
as  to  their  morphological  position.  The  question  as  to  the  relative 
morphological  position  of  the  crystalline  cone  cells  and  the  retinular 
cells  is,  however,  not  so  clear. 

According  to  Grenacher  the  ommatidium  is  two-layered,  and  the 
lens  and  cone  are  morphologically  distinct  from  the  retina.  If  this 
view  is  held,  then  the  question  stated  above  does  not  exist;  but  such 
an  interpretation  can  no  longer  be  held  on  comparative  anatomical 
or  embryological  grounds,  as  has  been  shown  so  well  by  numerous  in- 
vestigators, the  evidence  for  which  it  is  not  necessary  to  give  here. 
Suffice  it  to  say  that,  as  has  been  shown  previously,  the  ommatidium  of 
Apis  arises  from  a  one-layered  epithelium,  and  all  the  cells  are  morpho- 
logically equivalent.  Taking  into  consideration,  then,  only  such  views 
as  are  based  on  such  interpretations,  we  find  two  opposing  theories. 

According  to  Patten,  Kingsley  and  others,  the  crystalline  cone  is 
sometimes  continuous  with  the  rhabdome;  these  two  would  therefore 
be  the  morphological  centre  of  the  ommatidium,  while  the  retinula 
must  arise  from  cells  outside  this.  When  the  crystalline  cone  is  not 
continuous  with  the  rhabdome,  Patten  still  considers  the  cone  as  the 
centre,  since  he  describes  processes  running  from  each  cone  cell  around 
the  rhabdome  but  inside  the  retinula  (as  in  Vespa).  To  this  interpre- 
tation those  investigators  who  consider  the  crystalline  cone  as  the 
terminus  of  the  nerve  fibres  would  probably  agree.  On  the  other 
hand,  Watase  holds  that  the  ommatidium  is  a  morphological  invagina- 
tion of  which  the  retinula  is  the  centre,  and  the  cone  cells,  lens  cells 
(homologous  with  the  corneal  pigment  cells  of  Apis)  and  pigment  cells 
follow  in  the  order  named.  By  this  interpretation  the  rhabdome,  cone 
substance  and  lens  are  homodynamous.  These  two  views  seem  in  no 
way  reconcilable,  and  more  investigation  is  necessary  to  decide  between 


1905.]  NATURAL   SCIENCES    OF   PHILADELPHIA.  139 

them,  since  it  scarcely  seems  probable  that  both  plans  exist,  since  all 
ommatidia  are  probably  the  result  of  one  kind  of  development. 

Patten  bases  his  view  on  the  fact  that  the  cone  cells  are  continuous 
with  and  part  of  the  rhabdome,  but  surely  in  Apis  there  is  no  such 
continuity,  since  all  through  the  development  they  are  separate,  and  in 
the  adult  eye  there  is  a  sharp  line  of  demarcation  between  them,  and 
they  also  react  very  differently  to  stains.  In  Vespa,  Patten  admits 
that  the  rhabdome  is  not  continuous  with  the  crystalline  cone  cells,  but 
in  this  case  he  describes  processes  between  the  rhabdome  and  retinula 
which  correspond  to  the  processes  which  form  the  rhabdome  in  other 
forms.  Since,  as  will  be  discussed  later,  the  rhabdome  is  really  part 
of  the  retinula,  being  formed  as  an  intracellular  secretion,  any  such 
process  from  the  cone  cells  would  have  to  pierce  the  retinula  cells  to 
occupy  such  a  position.  No  such  processes  occur  in  Apis.  If  such  a 
view  be  held  because  it  is  necessary  in  some  way  for  the  nerve  fibres  to 
reach  the  crystalline  cone,  on  the  assumption  that  the  nerves  end  there, 
such  a  necessity  disappears,  for,  as  will  be  shown  under  a  discussion 
of  the  innervation  of  the  ommatidium,  the  cone  is  in  no  way  a  nerve 
terminus.  Such  a  theory  of  innervation  does  not  seem  justified  for 
any  ommatidium,  and  therefore  the  necessity  for  this  conception  of 
the  morphology  disappears. 

On  the  other  hand  Watase  based  his  view  largely  on  the  eye  of 
Limulus.  This  view  commends  itself  on  account  of  its  extreme  sim- 
plicity, since  all  ommatidia  readily  lend  themselves  to  the  plan  of 
diagrammatic  representation  used  by  Watase  with  this  interpretation. 
Watase  seems  to  have  advanced  this  theory  rather  for  the  purpose  of 
giving  some  explanation  for  the  existence  of  the  rhabdome  than  for 
the  morphology  of  the  entire  ommatidium.  There  is,  I  think,  no  reason 
to  believe  that  the  rhabdome  was  ever  a  chitinous  substance,  and  in 
that  sense  it  is  not  homologous  with  the  lens.  In  the  ommatidium, 
as  we  now  know  it,  the  rhabdome  is  an  intracellular  secretion  full  of 
nerve  fibrils,  and  is  far  from  being  a  hard  chitinous  growth.  To  that 
extent,  then,  Watase's  conception  seems  an  error.  If,  however,  we 
look  on  the  lens,  cone  substance  and  rhabdome  as  secretions  (non- 
living protoplasmic  differentiations),  of  which  the  lens  only  is  an  extra- 
cellular secretion,  then  the  homology  may  hold.  Acording  to  this 
view,  then,  the  ommatidium  did  not  arise  as  a  pit  filled  with  chitin, 
but  rather  the  sinking  in  of  certain  cells,  with  a  corresponding  retention 
of  the  secretion  inside  the  cell,  has  taken  place  with  the  assumption  of 
new  functions.  Parker  has  argued  that  the  retinular  cells  cannot  be 
considered  as  homologous  with  the  lens  secreting  cells,  since  the  lens 


140  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

cells  secrete  on  their  distal  surface  while  the  retinular  cells  secrete  on 
their  lateral  surfaces.  My  observations  show  that  both  cone  cells  and 
retinular  cells  form  their  secretions  intracellularly  and  from  their  very 
positions  they  could  not  secrete  on  their  distal  surfaces,  but  this  does 
not  seem  to  me  to  be  any  objection  to  the  theory  of  Watase,  since  in 
the  invagination  of  the  cells  and  the  taking  on  of  new  functions  new 
forms  of  metabolic  activity  might  easily  be  acquired. 

Since,  however,  in  the  embryonic  development  of  the  ommatidium  of 
the  bee  we  find  a  stage  in  which  the  retinula  is  formed  without  cone 
cells  on  the  distal  end  and  with  the  rhabdome  partly  formed,  the  only 
inference,  it  seems  to  me,  is  that  the  cone  arises  from  lateral  cells,  and 
the  corneal  and  outer  pigment  cells  are,  of  course,  still  more  peripheral. 
From  this,  then,  it  seems  to  follow  that  the  conception  of  Watase  con- 
cerning the  morphology  of  the  ommatidium  is  the  correct  one.  There 
is,  so  far  as  has  been  observed,  no  real  invagination,  but  such  a  thing 
would  scarcely  be  expected  in  so  compact  an  organ;  neither  have  I 
observed  the  actual  overgrowing  of  the  cone  cells,  but  the  conclusion 
seems  inevitable  that  the  retinula  is  the  centre  of  the  ommatidium. 

Some  compound  eyes  have  been  described  in  which,  in  the  adult  eye, 
the  retinular  cells  extend  outside  the  cone  to  the  lens.  Such  cases  are 
found  when  the  number  of  pigment  cells  is  reduced  or  when  they  are 
entirely  wanting,  and  it  is  safe  to  assume  that  the  distal  lengthening 
has  taken  place  secondarily,  late  in  development.  From  the  migration 
of  the  corneal  pigment  cells  of  the  ommatidium  of  the  bee,  to  be  de- 
scribed later,  we  see  that  a  late  rearrangement  is  possible,  and  it  seems 
more  plausible  to  assume  that  such  cases  are  a  secondary  modification 
rather  than  that  there  are  two  ground  plans  of  ommatidia,  one  of 
which  has  its  retinula  centrally  placed,  the  other  has  the  cone  cells 
inside  the  retinula  as  the  axis. 

The  retinular  spindle  of  the  larva  resembles  in  appearance  various 
sense  buds  throughout  the  animal  kingdom,  such  as  taste  buds  and 
lateral  line  organs  of  vertebrates,  the  aesthetes  of  Chitons,  etc.  These 
sense  buds  often  have  some  marked  differentiation  of  the  cytoplasm 
internally  to  enable  the  peripheral  organ  to  perform  its  function.  This 
similarity  is  more  than  superficial,  however,  for  the  method  of  innerva- 
tion  which  will  be  described  in  detail  later  is  from  the  sense  cell  toward 
the  central  nervous  system,  and  this  is  the  method  for  many  of  these 
sense  buds,  although  the  opposite  direction  of  fibres  is  described  for 
some  (e.g.,  taste  buds). 

It  is-^safe  to  assume  that  these  sense  buds  are  accumulations  of 
single  sensory  cells,  such  as  are  widely  known  (e.g.,  sensory  epithelial 


1905.]  NATURAL   SCIENCES    OF   PHILADELPHIA.  141 

cells  of  Lumbricus,  epithelial  sensory  cells  [Flemming's  cells]  of  Mol- 
luscs), giving  greater  efficiency  at  a  certain  spot,  and  that  the  internal 
differentiations  are  but  secretions  or  cytoplasmic  differentiations  due 
to  the  specialized  condition  of  the  cell.  Granting  these  facts,  then, 
sense  buds  are  homologous  of  necessity  only  in  their  origin  from  an 
epidermal  tissue,  although  the  homology  may  be  greater.  Since  sense 
buds  are  known  which  are  sensitive  to  touch,  taste,  smell,  sight  and 
vibration  waves,  it  seems  entirely  unnecessary  to  assume  that  a  light- 
perceiving  organ,  such  as  an  ommatidium,  has  arisen  as  a  modification 
of  some  other  kind  of  sense  bud,  rather  than  that  it  arose  as  an  accumu- 
lation of  epithelial  cells  already  sensitive  to  light. 

Since  we  know  that  single  cells  are  acted  upon  by  light  waves  (e.g., 
Protozoa),  and  that  epidermal  cells  often  give  rise  to  nervous  impulses 
when  acted  upon  by  light  (e.g.,  skin  of  the  earth  worm),  there  seems 
no  reason  for  assuming  that  the  ommatidium  has  arisen  other  than  by 
an  accumulation  of  such  sensitive  cells  and  then  by  invagination  a 
light-refracting  organ  has  been  formed  over  it.  Such  a  view  is  directly 
opposed  to  the  view  of  Patten  that  the  ommatidium  is  a  hair-bearing 
sense  organ.  As  will  be  shown  later,  his  theory  is  untenable  on  account 
of  the  absence  of  the  essential  structure  for  such  a  homology — the  hair. 
There  is  not  only  no  indication  of  such  an  organ  for  the  eye,  but  no 
need  for  such  a  complicated  theory  of  the  origin  of  these  organs,  since 
easy  transition  steps  from  a  single  cell  sensitive  to  light  to  the  omma- 
tidium are  obtainable  and  such  an  origin  seems  far  more  probable. 

Johansen  (1893),  in  his  description  of  the  development  of  the  eye  of 
Vanessa  urticcz  L.,  figures  and  describes  a  spindle-shaped  mass  of  cells 
which  is  the  ommatidium  of  the  pupa  when  two  days  and  one  hour  old. 
He  has  also  observed  the  same  spindle  mass  in  the  young  pupa  of 
Sphinx  euphorbia.  This  differs  from  what  I  have  described  for  Apis 
in  that  the  corneal  pigment  cells  and  cone  cells  lie  distal  to  the  retinula, 
and  I  am  led  to  conclude  that  he  has  observed  a  stage  just  after  the 
sinking  in  of  the  retinula,  a  stage  which  I  am  unable  to  describe  for 
Apis.  At  any  rate  his  conception  of  the  morphology  agrees  with 
mine,  since  the  retinula  is  in  the  centre  of  the  ommatidium  and  the 
cone  cells  and  corneal  pigment  cells  are  lateral  to  it. 

2.  Pupa. 

During  the  so-called  semi-pupa  stage,  just  after  the  larva  is 
sealed  up  by  the  workers  of  the  hive,  and  before  the  bee  is  a  complete 
pupa,  very  rapid  growth  takes  place,  and  the  eye  increases  still  more  in 
size  and  becomes  more  and  more  differentiated  until  at  the  beginning 


142  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

of  the  pupa  stage  proper  the  ommatidia  are  completely  formed.  The 
exact  method  by  which  this  differentiation  takes  place  is  difficult  to 
learn,  since  the  growth  at  this  time  is  so  very  rapid  that  it  is  practically 
impossible  to  get  all  the  stages.  The  head  of  the  insect  grows  very 
rapidly  and  the  eyes  keep  pace  with  it.  The  retinular  cells  become 
longer  and  broader,  and  the  retinulse  lie  closer  together.  The  cone  and 
corneal  pigment  cells  come  to  lie  at  the  distal  end  of  the  retinula  by 
the  method  previously  described.  When  the  pupa  stage  proper  is 
entered  upon,  the  area  of  the  eye  is  practically  that  of  the  adult  eye. 

The  various  stages  of  the  pupa  period  are  easily  distinguishable 
externally,  and  this  fact  is  of  great  value  in  the  selection  of  material. 
The  eye  is  first  white,  like  the  rest  of  the  body,  then  pink,  then  brown, 
and  finally,  as  the  other  parts  of  the  body  take  on  their  adult  colors, 
black.  These  changes  of  color  are  due  to  the  deposition  of  pigment 
in  the  various  cells  of  the  ommatidium,  pigment  in  the  corneal  pigment 
cells  being  red  in  color,  giving  the  first  color  externally,  and  the  darker 
pigments  of  the  other  cells  obscuring  this  color  at  a  later  period.  These 
changes  enable  one  to  choose  the  desired  material  by  simply  uncapping 
the  cells  containing  pupae  without  removing  the  bee  from  its  cell,  since 
the  head  is  always  toward  the  outside. 

From  this  stage  on  it  becomes  necessary  to  discuss  the  various  parts 
of  the  ommatidium  separately.  Such  a  method  tends  to  give  the  im- 
pression of  a  lack  of  continuity  in  mode  and  time  of  development,  but 
the  drawings  which  accompany  the  description  are  made  of  the  entire 
ommatidium,  and  these  will  show  the  relative  size  and  degree  of  devel- 
opment at  various  stages.  The  order  followed  is  from  the  retinula  to 
the  more  lateral  cells. 

a.  The  Retinula. — The  retinula  cells  are  eight  in  number  normally, 
but  numerous  ommatidia  are  observed  in  which  nine  cells  are  present. 
In  the  earliest  pupa  stage  (fig.  3)  these  cells  extend  from  the  proximal 
end  (apex)  of  the  cone  cells  to  the  basement  membrane,  and  each  cell 
has  a  protoplasmic  process  extending  through  the  openings  in  the  base- 
ment membrane  toward  the  optic  lobes,  which  later  functions  as  the 
nervous  connection  of  these  cells  with  the  cells  of  the  retinular  ganglion. 
At  this  time  the  only  indication  of  the  rhabdome  is  the  clear  space  at 
the  distal  end  which  was  described  for  the  larval  ommatidium;  its 
differentiation  has  gone  on  little,  if  any,  during  the  rearrangement  of 
cells.  The  cytoplasm  at  the  distal  end  of  the  cells  is  more  granular 
than  elsewhere,  and  by  the  time  the  eye  has  reached  the  stage  figured 
pigment  is  laid  down  around  the  forming  rhabdome.  This  is  the  first 
pigment  laid  down  in  the  ommatidium,  but  at  almost  the  same  time 


1905.]  NATURAL   SCIENCES   OF    PHILADELPHIA.  143 

the  corneal  pigment  cells  acquire  pigment.  The  spindle  shape  of  the 
retinula  so  marked  in  the  larval  condition  is  still  retained,  the  retinula 
being  widest  at  about  one-third  of  the  distance  from  the  cone  cells  to 
the  basement  membrane.  The  relatively  large  nuclei  of  the  retinula  at 
this  time  are  near  together,  and  in  no  definite  arrangement  in  the  thick- 
est portion  of  the  cell  group.  The  cytoplasm  of  the  cells  is  uniform 
except  as  described  for  the  distal  end,  and  the  cell  membranes  between 
the  various  cells  are  not  visible.  The  outside  boundaries  of  the 
retinula  group  at  this  time  and  all  through  development  mark  off  the 
retinula  from  its  surrounding  pigment  cells  very  sharply,  and  the 
difference  in  the  appearance  of  the  protoplasm  makes  it  impossible  to 
confuse  the  various  cells. 

The  portion  of  the  retinula  which  lies  between  its  thickest  part  and 
the  basement  membrane  is  a  strand  of  protoplasm  circular  in  cross- 
section  and  without  any  signs  of  differentiation.  As  the  basement 
membrane  changes  its  position,  by  a  process  to  be  described  later, 
coming  to  lie  near  the  optic  ganglion,  this  portion  of  the  retinula  be- 
comes longer,  and  the  changes  which  take  place  in  the  retina  consist 
of  the  making  over  of  this  strand  of  protoplasm  into  the  retinula  cells 
proper.  This  change  progresses  proximally  and  consists  in  the  widen- 
ing out  of  the  cells  with  its  accompanying  rhabdome  formation.  The 
nuclei  shift  as  the  retinula  enlarges  and  elongates  until  we  reach  a  con- 
dition (fig.  2)  in  which  two  of  them  are  at  one  level  and  the  other  six 
(or  seven)  are  at  a  lower  level  and  arranged  in  a  rosette. 

At  the  time  when  the  nuclei  are  arranged  in  this  manner,  the  most 
distal  portion  of  the  retinul,a  becomes  arranged  in  a  definite  rosette, 
caused  by  each  of  the  cells  forming  a  projection  which  shows  its  dis- 
tinctness from  the  others  in  the  group  in  cross-section.  This  arrange- 
ment also  progresses  proximally  until  in  the  adult  condition  it  is  found 
throughout  the  length  of  the  retinula.  At  the  same  time  the  inner 
portion  of  the  mass  becomes  still  more  differentiated,  and  in  the  stage 
just  mentioned  the  axis  of  the  distal  end  is  occupied  by  a  strand  of 
protoplasm  which  takes  the  iron  haematoxylin  stain  (the  future  rhab- 
dome) surrounded  by  a  clearer  protoplasm.  Outside  of  this  clear  area 
the  protoplasm  is  granular  and  pigment  deposition  takes  place  here, 
keeping  pace  with  the  inner  differentiations,  and  these  changes  also 
progress  toward  the  basement  membrane.  The  rhabdome  formation 
precedes  slightly  the  formation  of  the  clear  protoplasm  around  it,  and 
the  proximal  end  of  the  forming  rhabdome  shades  off  gradually  into 
the  surrounding  undifferentiated  cytoplasm. 

The  nuclei  gradually  move  inward  as  the  cells  assume  their  adult  form 


144  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

until  they  come  to  rest  at  about  one-third  of  the  distance  from  the 
cone  to  the  basement  membrane,  which  on  account  of  the  tapering  of 
the  retinula  is  at  about  the  centre  of  the  cell,  as  far  as  mass  of  cyto- 
plasm is  concerned.  One  of  the  nuclei,  however,  moves  proximally 
until  it  lies  about  half-way  between  the  other  nuclei  and  the  basement 
membrane.  Where  a  nucleus  is  present,  the  retinula  cell  is  slightly 
pressed  out,  encroaching  on  the  outer  pigment  cells,  and  the  upper 
nuclei  are  not  all  at  the  same  level.  The  one  nucleus  which  occupies 
a  more  proximal  level  is  separated  by  some  distance  from  any  of  the 
others,  however,  and,  owing  to  the  regularity  with  which  it  is  found, 
cannot  be  considered  as  due  merely  to  a  mechanical  shifting.  In  the 
older  stages  of  development  it  becomes  difficult  to  count  the  nuclei 
of  the  retinula  since  they  are  at  different  levels,  but  I  have  been  unable 
to  see  anything  which  would  lead  me  to  suspect  that  this  proximal  nu- 
cleus was  other  than  one  of  the  retinular  nuclei.  Neither  is  there  any 
indication  that  the  presence  of  this  nucleus  is  accountable  for  the  pres- 
ence of  nine  retinular  cells  in  some  ommatidia,  for  it  is  found  in  all 
ommatidia  and  the  nine-celled  condition  is  comparatively  rare. 

The  rhabdome  differentiation  proceeds  until  it  reaches  the  distal 
surface  of  the  basement  membrane  where  it  ends  abruptly.  In  the 
pupa  stages  I  am  unable  to  find  the  nerve  fibres  which  in  the  adult  eye 
run  parallel  with  the  rhabdome  and  send  fine  fibrillse  into  it.  It  will 
be  noticed,  however,  that  in  the  pupa  the  rhabdome  is  wider  and  not 
so  definite  in  outline  as  it  is  in  the  adult  eye,  and  the  nerve  fibrils  are 
no  doubt  included  in  this  darker  central  body  which  I  have  identified 
as  the  rhabdome.  Both  rhabdome  and  nerve  fibrillse  are  but  differen- 
tiations of  the  cytoplasm  of  the  retinula  cells  and  their  development 
takes  place  together.  The  rhabdome  is  probably  not  a  uniform  struc- 
ture, but  no  doubt  contains  a  mass  of  fibrillaB,  the  endings  of  the  nerve 
fibres.  I  am  unable  to  see  any  such  structures,  however. 

The  development  of  the  retinula  consists,  then,  in  the  changing  of 
the  sense-bud-like  spindle  of  the  larval  eye  into  a  long  column  of  cells 
with  a  clear  shaft  through  the  centre,  through  which  light  can  pass  to 
reach  the  nerve  endings  in  it.  From  the  previous  description  it  will 
be  evident  that  the  rhabdome  is  not  formed  by  processes  from  the  cone 
cells,  which  are  present  from  the  beginning  of  ommatidial  development, 
but  is  an  intracellular  differentiation  of  the  retinula,  there  being  a  sharp 
line  of  demarcation  between  the  cone  cells  and  rhabdome  throughout 
their  development. 

b.  The  Cone  Cells. — The  cone  cells  are  four  in  number,  and  in  the 
early  pupa  stage  (fig.  3)  the  cone  is  spindle-shaped  and  lies  directly 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  145 

distal  to  the  retinular  spindle.  The  nuclei  are  large  and  spherical, 
and  lie  slightly  distal  to  the  centre  of  the  cell.  The  cytoplasm  is 
granular,  especially  in  the  distal  portion  of  the  spindle,  and  the  cell 
membranes  are  well  marked. 

Very  soon  the  cytoplasm  begins  to  be  differentiated,  and  by  the  time 
the  pupa  has  reached  the  stage  figured  (fig.  2)  vacuoles  begin  to  appear 
in  the  proximal  end  of  the  spindle,  which  marks  the  beginning  of  the 
formation  of  the  clear  cone  substance.  The  cells  now  increase  in  size 
considerably,  and  at  the  same  time  the  number  of  small  vacuoles 
increases.  Later  these  vacuoles  unite,  and  finally  a  condition  is  reached 
in  which  the  proximal  end  of  each  cell  is  occupied  by  one  large  clear 
vacuole.  The  cell  boundaries  remain  distinct  and  a  thin  layer  of 
granular  protoplasm  remains  surrounding  the  vacuole,  so  that  it  is 
strictly  an  internal  secretion  and  not  to  be  interpreted  as  a  secretion 
poured  out  on  the  inner  face  of  each  of  the  cells.  This  process  of  differ- 
entiation or  intracellular  secretion  goes  on  until  the  nuclei,  which 
decrease  in  size  and  become  long  and  narrow,  are  pushed  to  the  distal 
and  lateral  portion  of  the  cell,  where  they  remain  in  the  adult  eye. 
These  nuclei  are  filled  with  fine  chromatin  granules.  The  cone  in  the 
meantime  becomes  wide  at  the  distal  end,  and  elongates  very  much  to 
assume  its  true  cone  shape,  and  all  that  remains  of  the  original  cyto- 
plasm is  an  extremely  thin  sheet  all  around  the  cone.  I  am  inclined 
to  attribute  the  descriptions  by  some  authors  of  nerve  fibrils  on  the 
cone  to  the  shrinking  of  this  thin  film  under  certain  fixatives.  There 
is  no  nervous  connection  with  the  cone,  nor  does  it  appear  to  have  any 
function  save  transmitting  light  rays  to  the  sensitive  retina. 

There  is  no  indication  of  any  prolongation  of  the  cone  proximally, 
either  to  form  the  rhabdome,  as  previously  described,  or  to  form  proto- 
plasmic processes  surrounding  the  rhabdome  inside  the  retinula  cells,, 
such  as  Patten  describes  for  Vespa.  Such  fibres  could  not  exist  unless- 
they  were  to  pierce  the  retinula  cells,  since  the  rhabdome  is  really  a. 
part  of  the  latter;  and  since  the  cell  boundaries  of  the  cone  and  retinula 
are  so  well  marked  I  feel  sure  that  no  such  ingrowth  occurs. 

Equally  unsuccessful  has  been  a  search  for  any  additions  to  the  cone 
at  the  distal  end.  In  his  work  on  the  embryology  of  the  eye  of  Vespa, 
Patten  describes  a  layer  of  cells  distal  to  the  cone  which  arose  by  an 
overfolding  of  the  sides  of  the  entire  eye,  and  which  gave  rise  to  the 
lens.  In  a  later  paper  (1890)  he  disposes  of  his  invagination  theory,  but 
describes  a  pouring  out  of  chitin  from  the  distal  end  of  the  cone,  which 
secretion  he  mistook  for  the  layer  of  nuclei  at  an  earlier  time.  From 
my  examination  of  Apis  material  I  am  unable  to  find  anything  which 


146 


PROCEEDINGS  OF  THE  ACADEMY  OF 


[Feb., 


could  be  mistaken  for  nuclei  in  that  position  (unless  it  be  the  corneal 
pigment  cells  which  are  lateral  to  the  distal  end  of  the  cone)  or  for 
chitinous  secretion  of  the  cone;  and  for  this  insect  eye,  at  any  rate,  I 
am  led  to  doubt  the  validity  of  his  homology  of  such  a  structure  with 
the  pseudocone  of  ommatidia  of  the  "pseudocone  type,"  since  the 
distal  end  of  the  cone  is  perfectly  well  defined  at  every  stage  observed. 
The  differentiation  of  the  cone  consists  in  a  transformation  of  a  cone 
without  any  refractive  secretion  into  one  in  which  this  secretion  fills 
all  the  cells  proximal  to  the  nuclei,  or,  in  other  words,  a  modification 
of  an  acone  condition  into  an  eucone  condition,  to  use  terms  introduced 
by  Grenadier  for  adult  conditions  of  some  eyes.  There  can  be  no 
doubt  that  this  was  the  course  taken  during  the  evolution  of  the  eucone 
ommatidium.  Similarly,  Hickson  has  shown  that  the  so-called  pseudo- 
cones  described  for  many  insect  eyes  are  but  instances  in  which  the 
secretion  has  accumulated  in  the  distal  end  of  the  cone  rather  than  in 
the  proximal  end.  While  the  distinction  drawn  between  these  three 
kinds  of  cones  is  justifiable,  yet  there  seems  nothing  to  oppose  the  view 
that  they  are  but  modifications  of  one  primitive  type.  The  acone 
ommatidia  have  no  clear  refractive  substance  differentiated  in  the  cone 
cells,  and  are  considered  as  the  primitive  type  of  eye.  The  pseudocone 
cones  with  the  differentiation  of  clear  cone 
substance  distal  to  the  nuclei  and  the  eucone 
cones  with  a  proximal  secretion  are  but  modifi- 
cations of  the  primitive  type. 

c.  The  Corneal  Pigment  Cells  and  the  Lens. — 
The  lens  is  secreted  by  the  two  cells  which 
have  been  designated  corneal  pigment  cells. 
In  the  very  earliest  pupa  stage  these  cells  lie 
distal  and  lateral  to  the  cone  cells,  and  since 
they  are  thus  placed  at  this  time,  and  since 
their  secretion  product  is  distal  to  the  cone, 
they  are  next  in  order  in  going  out  from  the 
axis  of  the  typical  ommatidium. 

Before  these  cells  begin  their  secretion,  how- 
ever, the  nuclei  migrate  down  the  sides  of  the 
spindle-shaped  cone  and  come  to  lie  around 
the  apex  of  the  cone.  The  cause  of  this  mi- 
gration is  probably  purely  mechanical,  viz.,  the 
enlargement  laterally  and  distally  of  the  cone ; 

at  the  same  time  the  nuclei  are  thus  brought  nearer  to  the  source  of 
nutriment.     As  this  shifting  takes  place  the  nuclei,  originally  ovoid, 


H».-p.c 


ret. 


Fig.  6. — Young  pupal 
ommatidium  at  time  of 
migration  of  corneal 
pigment  nuclei. 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  147 

become  crescent-shaped,  and  finally  almost  encircle  the  apex  of  the 
cone.  Strands  of  cytoplasm  connect  the  nucleated  portion  of  the  cell 
with  the  distal  portion,  which  remains  at  the  point  where  secretion  is 
to  take  place.  As  the  cone  enlarges  and  the  cell  substance  of  the  cor- 
neal  pigment  cells  is  used  up  in  the  secretion  of  the  lens,  the  portion 
distal  to  the  cone  becomes  reduced  until  in  the  adult  eye  it  is  almost 
entirely  absent. 

Almost  immediately  after  pigment  is  first  formed  in  the  retinula  cells, 
it  begins  to  be  deposited  in  these  corneal  pigment  cells.  Owing  to  the 
fact  that  the  retinula  pigment  is  at  first  small  in  quantity,  and  since 
there  is  none  in  the  outer  pigment  cells  at  this  time,  the  pigment  of 
these  distal  pigmented  cells,  which  is  red,  gives  a  pink  color  to  the  en- 
tire eye  in  the  early  stages,  rather  than  the  brown  or  black  color  pos- 
sessed by  the  other  pigment,  as  is  true  in  late  stages. 

The  granules  of  pigment  are  large  and  red  in  color,  and  when  treated 
with  depigmenting  mixtures  do  not  disappear,  but  become  somewhat 
lighter  in  color. 

The  lens  is  secreted  by  these  cells  in  much  the  same  way  as  is  ordinary 
chitin  over  the  entire  body  of  the  bee.  This  chitinous  covering  is 
deposited  in  layers  which  are  easily  visible  in  the  adult  lens.  In 
addition  to  these  cells  the  outer  pigment  cells  also  seem  to  enter  into 
this.  In  the  pupal  eyes  before  any  chitin  is  deposited  by  the  corneal 
pigment  cells  thin  sheets  of  chitin  extend  out  from  the  outer  pigment 
cells,  and  since  these  cells  are  arranged  at  their  distal  ends  in  a  nearly 
hexagonal  manner  a  cross-section  of  these  plates  shows  the  future 
boundaries  of  the  facets.  In  the  adult  eye  the  portion  of  the  cornea 
which  directly  overlies  the  outer  pigment  cells  differs  slightly  from  the 
part  directly  over  the  cone  in  refractive  index  and  in  general  appear- 
ance, so  that  I  think  it  probable  that  the  space  between  these  sheets  of 
chitin  in  the  larva  is  filled  by  a  secretion  of  the  outer  pigment  cells. 
If  this  be  true,  then  every  cell  which  enters  into  the  formation  of  the 
compound  eye  has  to  do  with  some  sort  of  secretion,  either  intra-  or 
extracellular. 

The  structure  of  the  chitin  laid  down  by  the  corneal  pigment  cells  is 
not  uniform,  the  outermost  layer  being  more  dense  than  the  rest,  with 
a  decided  tendency  to  take  up  an  iron  hsematoxylin  stain,  the  middle 
or  main  portion  being  arranged  in  alternating  layers  of  different  den- 
sity, and  the  inner  portion  taking  a  protoplasmic  stain,  such  as  cosine 
or  Bordeaux  red. 

From  this  description  it  will  be  seen  that  the  corneal  pigment  cells 
(Hauptpigmentzellen,  pigment  cells  of  the  first  order)  are  homologous 


'       •     "  '    "..          -      :   "    :    ;:  .-~^.  •  '.'.:'.  :•...  .   :•.':'•  ~  ~~~  ' 

':'    -       _:.   :.  .    •-    -'•  :  :.  .    :;-;-   -~    ... 


_•     .--.--  .    r.  :  •'.         --  -•-:---•-  -  :.  :  :".   .      :-r.  \ 

-:  -  -    -     .-•".   -  :-:--    -  .-.:    1:-*       ".".-..--    :'..: 

.  :  \     --    '        -  .  :r.    •  ^>  .vr:  —  -   -.-       Ir  :.;.-: 
ete.  (Heaaer  1901), 
two  edk  are  f>mM.  and  otmyj  a  ««iJ»»-  poatim  or  mar  be 

-  -  .  --     :  -   —  -  >^  -:     ,-•:----;  -..: 

twt>  types  of  eocnpcande^^     On  the  otter  band,  the  compoaad 

;--  '-   ::   ::-    ;'  "   -y:  .-;--.   .       v      --  :   y  ._-  ::_  :::   ;•.-:'_-     :'-::;  dr;: 

ader  (carmcal  pigment  cdfe),  and  do  no*  have  the  conical  hjpodeimal 

I.--:  ...         -    -  -    -  :-  :  ; 


•••••  ao.  cxaiHaaauQB.  of  adasfc  eycst,  and  coustdcxGd  •****  DQHBK 
bylb*£actlbatJcdtfBambaddaiaribedtbeKpcBva« 

•  - -H-:  -._--;.-  -     -  .-  :-.-  i:.  -'i :'.;.-  --^j'v       "-'..:.:;-.:  i  ii-i 

:-  .      -         :    :-.r.      .::.'      .  -..    '.  :_-  ::•:::: 

_  -     -          -      _.  .  .   ..    .  .  . M.  -_..-_ 

".    _-    :  :?  ...  v._-   : :^-    '.:_-.    :••-.-?  :.r:   ":~ 
p^molafebae] 


;•        "  -  ->•--;•..-  ._    ___   '.:•-/  3,.-  :   ;  — 

aad  %HCS  the  irfls  as  bt^g  aeoeted  bj  ttecoaeedk.     It  has 

_   ._"        -        yj  _  _          .  _  .          „  •  ___  »      *     ji  _  __  m  _  jt  y  ____     *^ 

.  -      .       .          ..--     .  ^.  _:   ri:i  :__:  rr.-:  d"i:~  L; 

^r4-     lB,A^3^         ^-p^^I      -^MS.      •  wMftXI      «LM«»1.A-     C*M>  -  * 

•*  jcae*,.  ana  we  iBajr  veil  <MHH,HI  ns  OGnDutcnce  m 

Ii  1  .    .      ij    1  1          lr.:r-->  -.1     --  •;-:.-::  :.-  '.T^     ;--; 


ovaioofaod  tbe  ponitioai 


—  _.-,:•?:    :-.  1=  :?•:-  -     ^-..--  :/.:--   -,.:• 

arevbat 
Tbey.Kealtbe 

-_"."_-  _-  --.  -   _"  -_.  .  _       **       *   -  tf9    _  .   '  .""_', 

...—  .  •      -  -       ~\,.\      _  ••      •  __:  ._      .•  •  _-  . : . .:_ 

:'   .--      -    -  -  ::_  --  ir     .    --:r.  ;••:•::    :.  -   :_.     :v-;s 

T&wrjfHqaariJytiMso 


-,   ±1 
tbe  leas,  no: 

:•:-:   -        ..-  ._     -  -     ..:_  i.  -•:  -\- 

to  Be  at  abort  its 


1905.]  NATURAL   SCIENCES   OF    PHILADELPHIA.  149 

Pigment  is  deposited  in  these  cells  quite  early,  but  not  until  after 
it  has  appeared  in  both  the  retinular  and  corncal  pigment  cells,  and  is 
most  abundant  at  the  two  ends  of  the  cell.  It  will  be  noticed  that  of 
all  the  cells  of  the  eye  which  contain  pigment  none  acquire  this  until 
they  have  begun  to  form  the  secretion  to  which  they  give  rise.  The 
rhabdome  is  the  first  secretion  formed,  and  pigment  first  appears  in 
the  retinula;  later  the  lens  secretion  appears,  and  then  pigment  appears 
in  the  secreting  cells,  indicating,  it  seems  to  me,  that  this  pigment  is 
of  the  nature  of  a  by-product,  although  it  is  of  itself  of  value.  From 
one  point  of  view,  pigment  itself  is  a  secretion,  but  the  accumulation 
of  pigments  often  accompanies  other  secreting  activities.  Concerning 
any  possible  movements  of  the  pigment  under  different  light  conditions, 
no  observations  have  been  made. 

In  the  region  where  the  basement  membrane  is  formed  these  cells  are 
deeply  pigmented,  and  the  line  of  demarcation  from  the  cell  below  is 
very  marked.  At  this  point,  also,  and  only  here,  the  cells  are  fused 
with  the  retinular  elements.  This  intimate  union  can  exist  only  when 
the  retinular  elements  have  filled  out  to  that  point,  since  in  the  pupal 
stages  that  portion  of  the  retinula  is  a  thin  strand.  The  retinular  cells 
here  are  also  deeply  pigmented. 

3.  The  Adult  Ommatidium. 

In  the  discussion  of  the  changes  which  take  place  during  the  pupal 
period  many  of  the  details  of  the  adult  ommatidia 
are  given,  and  to  avoid  unnecessary  repetition  only 
such  things  as  have  been  omitted  will  be  discussed 
here. 

a.  The  Retinula. — The  adult  retinular  cells  are 
extremely  complicated  structures,  due  to  the  fact 
that  each  cell  has  so  many  differentiations  inter- 
nally. The  central  part  of  each  cell  is  differentia- 
ted into  a  sector  of  the  rhabdome,  which  is  possi- 
bly a  dead  secretion,  but  of  this  there  is  room  for 
some  doubt.  Outside  the  rhabdome  is  an  area  of 
clear  protoplasm  in  which  the  nervous  elements  of 
the  cell  are  found,  and  still  outside  of  this  is  the 
granular  portion  of  the  cell  in  which  pigment  gran- 
ules are  found.  Each  of  these  cells  then  secretes 
part  of  the  rhabdome,  acts  as  a  pigment  cell  by 
the  accumulation  of  pigment  on  its  outer  surface,  and  is,  in  addition,  a 
nerve-ending  cell. 


c.c. 


Fig.  7. — Diagram 
of  part  of  omma- 
tidium,  showing 
apex  of  cone  and 
distal  end  of  re- 
tinula. 


150  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

The  innervation  of  the  ommatidium  is  a  question  over  which  there 
has  been  much  discussion,  and  various  views  have  been  put  forth.  The 
views  can,  however,  be  classed  into  two  groups :  those  which  make  the 
cone  cells  the  nerve-ending,  and  those  which  find  the  terminations  in 
the  retinula.  It  has  been  shown  conclusively  by  numerous  investiga- 
tors that  the  cone  has  nothing  whatever  to  do  with  receiving  light 
stimuli,  and  it  would  be  useless  to  take  up  the  arguments  against  this 
view,  any  more  than  has  been  done  in  showing  that  in  the  development 
the  cone  and  rhabdome  are  separate. 

Those  who  hold  that  the  retinula  is  the  nerve-ending  of  the  omma- 
tidium have  not  always  been  able  to  show  in  a  satisfactory  manner 
just  how  this  innervation  takes  place.  On  this  point  two  views  have 
been  held:  (1)  that  the  retinula  is  innervated  by  nerve  fibrils  from 
the  retinular  ganglion  which  run  into  the  retinular  cells  or  rhabdome,  or 
(2)  that  the  retinular  cells  are  themselves  ganglionic  epidermal  cells 
which  send  in  nerve  fibres  to  the  retinular  ganglion.  From  the  de- 
scription which  has  preceded  it  is  evident  that  the  second  of  these 
views  is  the  one  here  held  for  the  eye  of  the  bee.  Before  going  into  a 
detailed  descripton  of  the  nervous  elements  in  the  cells  concerned, 
let  us  first  examine  the  problem. 

In  the  first  place,  it  seems  reasonable  to  assume  that  during  the 
course  of  the  evolution  of  light-perceiving  organs  the  first  condition 
was  that  in  which  certain  cells  of  the  hypodermis  became  sensitive  to 
light,  or  possibly  heat,  through  the  accumulation  of  pigment  or  some 
other  change  in  the  cytoplasm.  Such  cells  would  arise  before  there 
were  any  cells  in  the  central  nervous  system  to  receive  their  nerve 
stimuli,  and  it  may  be  assumed  without  danger  that  such  cells  would 
send  in  processes  to  the  centrally  placed  nerve  cells,  when  the  time  for 
nerve  connections  arrived,  rather  than  that  the  nerves  arose  from  the 
central  nervous  system.  In  other  words,  the  peripheral  nervous 
system  is  older  than  the  central  nervous  system  which  elaborates  the 
impulses,  and  on  hypothetical  grounds,  a  basis  which  is  rather  unsafe 
in  zoology  unless  backed  up  by  observations,  we  may  assume  that  the 
innervation  is  centrad. 

From  the  standpoint  of  embryology,  we  find  that  the  eye  epidermis 
is  formed  and  even  the  ommatidia  are  differentiated  before  the  retinal 
ganglion  cells  have  assumed  their  adult  position  or  are  connected  with 
the  optic  ganglia.  Not  only  that,  but  the  strands  of  cytoplasm  which 
become  the  nerves  of  the  ommatidia  arise  from  the  retinula  cells 
and  grow  centrad. 

In  the  adult  condition  we  find  that  the  nerve  fibres  are  continuous 


1905.]  NATURAL    SCIENCES    OF    PHILADELPHIA.  151 

with  the  cytoplasm  of  the  retinula  and  run  to  the  retinular  ganglion, 
where  they  surround  the  nuclei  of  the  ganglionic  cells.  There  is  no 
indication  of  long  nerve  processes  from  the  ganglion  cells  toward  the 
eye. 

The  nervous  elements  of  the  retinular  cell  proper  consist  of  a  differ- 
entiated portion  of  the  cytoplasm  inside  the  clear  area  which  lies  out- 
side the  rhabdome.  This  nerve  fibre  can  be  seen  best  in  sections  stained 
in  iron  hsematoxylin,  where  it  stains  black.  From  this  fibre,  which 
starts  at  the  distal  end  of  the  cell  and  runs  parallel  to  the  rhabdome, 
smaller  fibrils  are  given  off  which  run  into  the  rhabdome  where  they  all 
end.  More  properly  speaking,  these  fibrils  are  further  differentiations 
of  cytoplasm  which  lies  between  the  main  fibril  and  the  centre  of  the 
retinula.  These  fibrils  extend  from  the  fibre  to  the  rhabdome  along 
the  whole  length  of  the  retinula  proper,  so  that  the  nerve-endings  are 
very  numerous.  Below  the  basement  membrane  these  main  fibres  can 
be  traced  as  dark  lines  in  the  centre  of  the  protoplasmic  processes  to 
the  retinular  ganglion.  All  of  these  fibres  are  best  seen  on  cross- 
sections  where  they  stand  out  as  black  dots,  but  they  can  also  be  seen 
on  longitudinal  sections.  It  is  probable  that  the  cause  of  the  black 
color  of  the  rhabdome  in  sections  stained  with  iron  haematoxylin  is  the 
presence  of  these  numerous  nerve  fibrils.  Concerning  the  distribution 
of  these  fibrils  inside  the  rhabdome,  I  am  unable  to  say  anything  defi- 
nite, but  they  probably  extend  almost  straight  to  the  centre.  In 
material  fixed  in  Kleinenberg's  picro-sulphuric  fixing  fluid  the  rhab- 
dome sometimes  appears  as  a  tube,  and  this  may  indicate  that  these 
fibrils  do  not  run  all  the  way  to  the  centre.  While  the  innervation  of 
the  ommatidium  is  under  discussion,  it  might  be  stated  that  there  is  no 
indication  of  nervous  connection  with  any  of  the  other  cells  peripheral 
to  the  retinula. 

The  significance  of  the  single  retinular  nucleus  which  lies  at  a  lower 
level  than  the  others  of  each  ommatidium,  is  somewhat  hard  to  explain. 
Hickson  held  that  some  of  the  retinular  cells  of  Musca  had  more  than 
one  nucleus.  In  this  form  there  are  three  layers  of  nuclei  in  place  of 
two,  as  in  Apis,  Hesse,  on  the  contrary,  homologizes  these  lower 
nuclei,  only  one  of  which  is  present  in  Apis,  with  the  proximal  retinular 
cells  of  the  apterygote  insect  eyes.  In  these  forms  the  retinula  is 
divided  into  two  parts,  one  distal  to  the  other,  each  of  which  acts  alone 
in  the  formation  of  rhabdome  structure,  and  both  have  nerve  fibre 
connections  with  the  optic  ganglia.  A  similar  condition  is  found  in 
some  pterygote  insect  ommatidia.  Of  these  two  views  the  one  of 


152  PROCEEDINGS   OF   THE   ACADEMY   OF  [Feb., 

Hesse  seems  more  probable.  As  Hickson  says,  there  is  nothing  mor- 
phologically wrong  with  the  supposition  that  certain  cells  are  multi- 
nucleate;  but  since  the  explanation  of  Hesse  helps  us  to  complete  the 
homologies  of  the  cells  of  the  ommatidia  of  the  various  groups,  it 
seems  to  have  more  weight. 

The  question  as  to  the  method  of  modification  in  number  of  retinular 
cells  during  the  course  of  evolution  is  an  interesting  one,  but  it  must  be 
admitted  that  as  yet  very  little  is  known  concerning  it.  It  seems  not 
unlikely  that  the  ommatidium  of  the  bee  is  changing  cither  from  eight 
to  nine  retinular  cells,  or  from  nine  to  eight,  since  it  is  rather  rare  for 
the  number  of  these  elements  to  be  variable.  The  thought  has  sug- 
gested itself  that  possibly  this  one  proximal  nucleus  was  one  which  was 
in  the  process  of  delamination  from  the  ommatidial  epidermis,  and  was 
therefore  tending  toward  a  reduction  of  retinal  elements,  but  this  does 
not  seem  to  be  as  probable  an  explanation  as  that  of  Hesse.  It  may 
be  said,  however,  that  Johansen  describes  the  ommatidium  of  Vanessa 
as  having  seven  retinular  cells  and  two  retinal  ganglion  cells,  while 
in  Apis  there  is  probably  but  one  retinal  ganglion  cell  to  each  omma- 
tidium and  at  least  one  more  cell  in  each  retinula. 

VII. — HOMOLOGIES  OF  COMPONENT  PARTS. 

The  question  of  homologies  of  the  various  eyes  of  the  invertebrates 
has  excited  much  discussion,  but  since  only  compound  eyes  have  been 
investigated  in  this  paper,  this  problem  will  not  be  taken  up  here. 
The  question  of  the  homology  of  the  different  kinds  of  compound  eyes 
is  worthy  of  consideration.  Such  eyes  occur  in  Crustacea  and  insects,4 
and  a  comparison  of  the  groups  indicates  that  there  is  here  either  uni- 
formity of  origin  and  plan  or  one  of  the  most  remarkable  cases  of  con- 
vergence known  in  the  animal  kingdom.  The  essential  part  of  the 
ommatidium  is  the  retinula,  and  this  may  be  considered  as  a  sense  bud, 
formed  by  the  accumulation  of  cells  sensitive  to  light,  which  has  been 
modified  internally  to  aid  in  light  perception.  Since  such  groups  of 
cells  occur  throughout  the  whole  animal  kingdom  and  associated  with 
all  the  senses,  there  is  nothing  remarkable  about  the  similarity  so  far. 
In  addition  to  the  retinula,  an  ommatidium  consists  of  a  cone  and  a 

4  No  account  of  the  so-called  compound  eyes  of  myriapods  and  arachnids  is 
taken  here,  since  their  plan  is  so  different  that  they  cannot  readily  be  homologized 
with  those  of  crustaceans  or  insects.  Until  we  know  more  of  the  comparative 
embryology  of  these  forms  it  may  be  as  well  to  suspend  judgment.  I  do  not  feel 
qualified  to  include  these  in  the  present  discussion,  but  evidently  from  the  re- 
searches of  numerous  investigators  we  may  conclude  that  the  homology  is  not  as 
close  as  in  the  forms  under  discussion. 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  153 

chitinous  covering  which  may  be  faceted,  and  possibly  accessory  cells 
occur  between  ommatidia  which  act  as  pigment  cells.  In  order  that 
the  light  rays  may  be  centred  on  the  retinular  nerve  fibres,  some 
refractive  organ  must  be  present  above  it  (the  cone)  and  the  whole 
organ  must  be  covered  by  chitin,  as  is  the  rest  of  the  body.  This  chitin 
in  turn  may  assist  in  the  refraction,  as  it  does  in  many  cases,  or  may 
even  secondarily  assume  the  functions  of  the  cone  entirely  if  no  cone 
substance  is  differentiated  (acone  eyes).  For  the  occurrence  of  these 
parts  there  are  but  two  explanations :  either  they  are  differentiations 
of  cells  which  formerly  lay  outside  the  retinula  group,  and  have  been 
placed  distal  to  it  to  assist  in  collecting  light  rays  to  form  a  more  perfect 
image,  or  they  have  been  placed  distal  to  the  retinula  by  the  differentia- 
tion of  some  other  cell  layer  which  has  been  superimposed. 

The  various  cells  of  the  ommatidium  seem  to  lend  themselves  to 
homologies  very  readily.  The  retinulse  of  the  various  ommatidia  are 
groups  of  cells  which  are  the  nerve  endings  of  the  eye,  and  all  ommatidia 
agree  in  this  respect.  Retinulse  of  apterygote  insects,  some  Crustacea 
and  a  few  pterygote  insects  have  two  layers  of  retinular  cells,  while 
others  have  but  one,  but,  as  was  pointed  out  for  Apis,  the  position  of 
nuclei  at  different  levels  in  the  higher  insects  may  indicate  a  remnant 
of  a  former  two-layered  condition  for  these  retinulae  also.  In  other 
words,  the  morphological  invagination  by  which  the  insect  eye  has 
arisen  may  be  carried  farther  in  some  cases  than  in  others.  Hickson 
has  shown  that  acone,  pseudocone  and  eucone  cones  are  probably 
homologous,  and  the  fact  that  some  cones  are  composed  of  but  two 
cells  while  others  have  four  seems  a  matter  of  small  moment.  The 
probable  homology  of  the  corneal  hypodermal  cells  of  apterygote  in- 
sects and  Crustacea  with  the  corneal  pigment  cells  of  most  pterygote 
insects  has  been  dwelt  on  sufficiently  and  is  held  on  comparative  ana- 
tomical grounds  by  Hesse.  The  accessory  pigment  cells  are  undoubt- 
edly but  undifferentiated  cells  of  the  layer  of  epidermis  from  which  the 
retinulae  arise,  and  their  presence  or  absence  is  of  small  importance  in 
homologizing  the  different  ommatidia.  The  fact  also  that  mesodermal 
cells  may  migrate  to  a  position  between  ommatidia,  as  is  held  for  some 
eyes,  is  also  of  small  consequence.  As  far,  then,  as  the  component  parts 
of  the  ommatidia  are  concerned  there  is  no  difficulty  about  establishing 
a  very  close  homology,  and  this  similarity  is  considerably  strengthened 
by  showing  that  the  corneal  pigment  cells  are  not  only  similar  in  func- 
tion to  the  corneal  hypodermal  cells,  but  that  at  an  early  stage  they 
actually  occupy  the  same  position. 

The  whole  question  seems,  then,  to  be  one  which  must  be  settled 


154  PROCEEDINGS  OF  THE  ACADEMY  OF  [Feb., 

from  embryological  evidence.  The  problem  is,  which  of  the  two 
methods  of  formation  previously  mentioned  is  the  method  which  actu- 
ally exists  in  ontogeny,  and  are  all  compound  eyes  formed  by  the  same 
method  ?  From  this  work  on  Apis  and  that  of  Johansen  on  Vanessa  it 
is  evident  that  the  differentiation  of  cells  outside  the  retinula  to  form 
cone  and  lens  layers  is  what  occurs  in  insects,  and  the  whole  question 
hinges  on  the  development  of  the  crustacean  eye.  Reichenbach  and 
Kingsley  describe  the  eye  as  arising  by  an  invagination;  and  if  either 
of  these  investigators  is  right,  although  they  differ  as  to  the  fate  of 
the  three  layers  formed,  then  the  compound  eyes  of  these  crustaceans 
are  not  homologous  with  the  compound  eyes  of  insects.  On  the  other 
hand,  Herri ck  insists  that  the  compound  eye  of  Alpheus  arises  from  a 
single  layer  of  epidermis,  and  according  to  this  view  the  homology 
holds.  Herrick's  view,  that  even  if  an  invagination  does  occur  it  is 
of  no  importance,  does  not  seem  tenable,  for  if  an  invagination  occurs 
then  cone  and  retinula  do  not  come  from  contiguous  cells,  and  that  I 
believe  to  be  a  matter  of  great  importance. 

From  the  striking  similarity  in  position  and  function  of  the  parts 
of  the  ommatidium,  and  from  the  observations  of  Herrick,  we  are  safe 
in  concluding  that  the  eyes  of  the  various  groups  under  consideration 
are  distinctly  homologous,  and  there  must  be  some  other  explanation 
for  the  invaginations  observed  by  the  other  writers  mentioned. 

The  interpretation  of  the  formation  of  the  ommatidium  which  is 
held  from  an  examination  of  the  eye  of  Apis  makes  possible  a  very 
close  homology  of  the  elements  of  the  compound  eye  with  the  ocelli 
of  insects,  such  as  was  held  by  Grcnacher;  and  this  homology  seems 
materially  strengthened  since  an  homology  can  be  shown  between 
the  corneal  pigment  cells  of  insect  ommatidia  with  the  chitin-secreting 
cells  of  the  ocelli.  An  objection  that  might  be  raised  is  that  the 
vitreous  body  of  the  ocellus  arises  from  cells  which  are  all  to  one  side  of 
the  retina  rather  than  from  all  sides,  but  since  they  are  adjoining  cells 
this  might  be  a  secondary  change.  From  sections  of  ocelli  of  the  pupae 
of  the  bee  which  have  been  examined,  it  is  evident  that  the  middle 
ocellus  arises  from  a  double  invagination,  indicating  a  fusion  of  two 
organs,  while  the  lateral  ocelli  arise  from  single  invaginations. 

VIII. — SUMMARY. 

The  primitive  arrangement  of  ommatidia  is  tetragonal  (p.  130). 
The  hairs  over  the  lens  are  secreted  by  bi-nucleated  hair  cells  with 
intracellular  ducts  which  lie  between  the  ommatidia  (p.  131). 

The  ommatidium  arises  as  a  group  of  cells  with  superimposed  nuclei, 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  155 

which  later  become  arranged  as  a  spindle  surrounded  by  smaller  cells 
(p.  136). 

This  spindle  is  the  retinula,  and  the  cone  cells  and  pigment  cells 
assume  a  distal  position  by  a  morphological  imagination  (p.  137). 

The  retinula  is  the  centre  of  the  ommatidium,  and  the  cone  cells, 
corneal  pigment  cells  and  outer  pigment  cells  follow  in  the  order 
named  (p.  141). 

The  ommatidium  is  composed  of  eight  or  nine  retinula  cells  around 
the  rhabdome,  four  cone  cells,  two  corneal  pigment  cells  and  about 
twelve  outer  pigment  cells  (p.  126). 

The  rhabdome  and  cone  arc  intracellular  secretions,  while  the  lens 
is  an  extracellular  secretion  of  the  pigment  cells  (p.  144). 

The  corneal  pigment  cells  are  homologous  with  the  corneal  hypoder- 
mal  cells  of  crustacean  and  apterygote  insect  ommatidia  (p.  147). 

The  innervation  of  the  ommatidium  is  by  a  differentiation  of  part  of 
the  retinular  cells  into  nerve  fibrils,  and  these  extend  to  the  retinular 
ganglia  (p.  149). 

The  lens  is  secreted  by  the  corneal  pigment  cells  which  early  in  the 
pupa  stage  lie  distal  to  the  cone,  and  possibly  also  by  the  outer  pigment 
cells  (p.  148). 

Pigment  is  formed  inside  all  the  cells  of  the  ommatidium,  except  the 
cone  cells,  by  a  cytoplasmic  differentiation  (p.  149). 

The  ommatidium  arises  from  a  strictly  one-layered  epidermis,  which 
passes  directly  from  the  larva  to  the  pupa  without  the  loss  of  any  cells 
or  additions  from  other  tissues  (p.  136). 

LITERATURE. 

BALFOUR,  F.  M.     1881.     A  Treatise  on  Comparative  Embryology,  II,  London. 
BUTSCHLI,  O.     1870.     Zur  Entwicklungsgeschichte  der  Biene.      Zeit.  /.  Wiss. 

Zool  XX,  pp.  519-564. 
CARRIERS,  J.     1884.     On  the  Eyes  of  Some  Invertebrates.     Qt.  Jr.  Micr.  Sc., 

XXIV,  New  Series,  pp.  673-81. 
1885.     Die  Sehorgane  der  Thiere  vergleichend  anatomisch  dargestellt. 

Mtinchen  und  Leipzig,  R.  Oldenbourg,  6  +  205  pp. 

1885.     Einiges  uber  die  Sehorgane  von  Arthropoden.     Biol.    Centralbl., 

V,  No.  19,  pp.  589T97. 

1886.     Kurze  Mittheilungen  aus  fortgesetzten  Untersuchungen  viber  die 

Sehorgane.     Zool.  Am.,  IX,  Nos.  217  and  230. 

FERNALD,  H.  T.     1890.     The  Relationships  of  Arthropods.     Studies  Biol.  Lab. 

Johns  Hopkins  Univ.,  IV,  pp.  431-513. 
GRENACHER,  H.     1874.     Zur  Morphologic  und  Physiologic  des  facettirten  Ar- 

thropodenauges.     Gottingen  Nachrichten,  pp.  645-56. 
1877.     Untersuchungen    iiber    das    Arthropoden-Auge.     Beilageheft    zu 

den  kHnischen  Monatsbldttern  fur  Augenheilkunde,  XV. 

1889.     Untersuchungen  iiber  das  Sehorgan  der  Arthropoden,  insbesonder 

des    Spinnen,    Insecten    und    Crustaceen.    Gottingen,    Vanderhoeck    und 
Ruprecht,     8  +  188  pp.,  11  Taf. 


156  PROCEEDINGS    OF   THE    ACADEMY   OF  [Feb., 

HERRICK,  F.  H.     1889.     The  Development  of  the  Compound  Eye  of  Alpheus. 

Zool.  Am.,  XII,  pp.  164-9. 
HESSE,  RICH.     1901.     Untersuchungen  iiber  die  Organe  den  Lichtempfindung 

bei  niederen  Thieren.     VII,  Von  den  Arthropoden-Augen.     Zeit.  f.  vnss. 

Zool.,  LXX,  pp.  348-473. 
HICKSON,  S.  J.     1884.     The  Eye  and  Optic  Tract  of  Insects.     Qt.  Jr.  Mic.  Soc., 

No.  98. 

1885.     The  Retina  of  Insects.     Nature,  XXXI,  pp.  441-2. 

JOHANSEN,  H.     1893.     Die  Entwicklung  des  Imagoauges  von  Vanessa  urticse  L. 

Zool.  Jahrbiich,  VI,  pp.  445-80. 

KENYON,  F.     1896.     The  Brain  of  the  Bee.     Jr.   Comp.  Neurology,  VI,  pp. 
133-210. 

1897.     The  Optic  Lobes  of  the  Bee's  Brain  in  the  Light  of  Recent  Neuro- 
logical Methods.     Am.  Nat.,  XXXI,  pp.  369-76. 

KINGSLEY,  J.  S.     1886.     The  Arthropod  Eye.     Am.  Nat.,  XX,  pp.  862-7. 

1886.     The  Development  of  the  Compound  Eye  of  Crangon.     Zool.  Anz., 

IX,  No.  234,  pp.  597-600. 

1887.     The  Development  of  the  Compound  Eye  of  Crangon.     Jr.  Morph., 


I,  No.  1,  pp.  49-66. 

LEYDIG,    F.     1855.     Zum    feineren    Bau    der    Arthropoden.     Arch.    f.    Anat., 
Physiol.  u.  wiss.  Med.,  pp.  376-480. 

1864.     Das  Auge  der  Gliederthiere.   Tubingen,  Laupp  und  Siebeck,  50  pp. 

LOWNE,  THOMPSON  B.     1878.     On  the  Modifications  of  the  Simple  and  Com- 
pound Eyes  of  Insects. 

1884.     On  the  Compound  Vision  and  the  Morphology  of  the  Eye  of  In- 
sects.    Trans.  Linn.  Soc.,  London. 

PARKER,  G.  H.     1891.     The  Compound  Eyes  in  Crustaceans.     Butt.  Mus.  Comp. 

Zool.  Harvard  Univ.,  XXI,  No.  2,  pp.  45-140,  10  plates. 
PATTEN,   WILLIAM.     1886.     Eyes  of  Molluscs   and  Arthropods.     Mitth.   Zool. 

Stat.  Neapel,  VI,  pp.  542-756. 

1887.     Studies  on  the  Eyes  of  Arthropods.     I.  Development  of  the  Eyes 

of  Vespa.     Jr.  Morph.,  I,  pp.  193-226. 

1890.     Is  the  Ommatidium  a  Hair-bearing  Sense-bud?     Anat.  Anz.,  V, 

Nos.  13,  14,  pp.  353-9. 

REICHENBACH,  H.    1886.  -Studien  zur  Entwickelungsgeschichte  des  Flusskrebses. 

Frankfurt. 
WATASE,  S.     1889.     On  the  Structure  and  Development  of  the  Eyes  of  the 

Limulus.     Johns  Hopkins  Univ.  Circ.,  VIII,  No.  79,  pp.  34-7. 

1890.     On  the  Morphology  of  the  Compound  Eyes  of  Arthropods.     Studies 

Biol.  Lab.  Johns  Hopkins  Univ.,  IV,  No.  6,  pp.  287-334. 

WILLEM,  V.     1897.     Les  yeux  et  les  organes  post-antennaires  des  Collemboles. 
Ann.  Soc.  entomol.  de  Belgique,  XLI,  p.  225. 


ABBREVIATIONS. 


I.,  lens. 

c.  p.  c.,  cornea!  pigment  cell. 
o.  p.  c.,  outer  pigment  cell. 
b.  m.,  basement  membrane. 
/.  ret.  n.,  lower  retinular  nucleus. 
ch.,  chitin. 

/.  b.,  facet  boundary. 
ret.  gang,  n.,  nucleus  of  retinular  gang- 
lion. 
br.  sh.,  brain  sheath. 


int.  d.,  intracellular  duct. 

c.  c.,  crystalline  cone. 

rhb.,  rhabdome. 

ret.,  retinula. 

pgm.,  pigment. 

n.,  nucleus. 

h.  c.,  hair  cell. 

tr.,  trachea. 

n.  /.,  nerve  fibre. 


1905.]  NATURAL   SCIENCES   OF   PHILADELPHIA.  157 

EXPLANATION  OF  PLATES  VI,  VII,  VIII. 

PLATE  VI,  Fig.  1. — Section  of  entire  eye  and  optic  lobes.  The  heavy  lines  show 
the  course  of  the  nerve  fibres  as  worked  out  by  Kenyon  (diagram- 
matic) . 

PLATE  VII,  Fig.  2. — Ommatidium  of  young  pupa  before  rhabdome  is  differenti- 
ated and  at  time  of  first  pigmentation  of  retinula  cells. 

Fig.  3. — Ommatidium  of  older  pupa,  showing  differentiation  of  rhabdome 
and  lens  formation. 

Fig.  4. — Cross-section  through  distal  end  of  cone  of  pupa  of  same  age  as 
fig.  2,  showing  corneal  pigment  cells. 

Fig.    5. — Cross-section  through  cone  of  older  pupa. 

Fig.  6. — Cross-section  through  proximal  end  of  cone  of  pupa  (same  stage 
as  figs.  3  and  5). 

Fig.    7. — Cross-section  through  cone  of  young  pupa. 

Fig.  8. — Cross-section  through  retinula  of  young  pupa  before  rhabdome 
formation. 

Fig.  9. — Cross-section  through  distal  end  of  retinula  of  young  pupa,  show- 
ing first  traces  of  pigment. 

PLATE  VIII,  Fig.  10. — Entire  ommatidium  (somewhat  diagrammatic).    Adult. 

Fig.  11. — Entire  ommatidium,  as  if  dissected  out,  without  outer  pigment 
cells  (diagrammatic).  Adult. 

Fig.  12. — Section  of  entire  ommatidium,  showing  distribution  of  pigment. 
Adult. 

Fig.  13. — Cross-section  just  proximal  to  lens,  slightly  oblique. 

Fig.  14. — Cross-section  through  extreme  distal  ends  of  retinulse  and  proxi- 
mal ends  of  cones,  slightly  oblique. 

Fig.  15. — Cross-section  through  retinulae,  showing  relation  of  outer  pigment 
cells  in  this  region. 

Fig.  16. — Cross-section  through  retinulse  in  region  of  nuclei. 

Fig.  17. — Cross-section  through  retinulse  in  region  of  proximal  nucleus. 

Fig.  18. — Cross-section  of  eye,  cutting  basement  membrane  parallel.  The 
distinctness  of  nerve  fibres  of  each  ommatidium  is  shown. 


PROC.  ACAD.   NAT.  SCI.  PH1LA.   19O5. 


PLATE  VI. 


'L  inner  ch. 


fm.3 


PHILLIPS.       EYE    OF    THE    HONEY    BEE. 


PROC.  ACAD.  NAT.  SCI.  PHILA.  19O5. 


PLATE  VII. 


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CrD.C.      $% 


ret.n. 


PHILLIPS.       EYE    OF    THE    HONEY    BEE. 


PROC.  ACAD.  NAT.  SCI.   PHILA.    1OO5. 


PLATE  VIII. 


ret. 


ret.n. 


—  bm. 


c-p.c. 


-rhb. 


-ret.n. 


; — bm. 


^.-ret. 

%* 


n.f.  ,„•. 


/3 


7V 


PHILLIPS.       EYE    OF    THE    HONEY    BEE. 


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23FEB'68 


LIBRARY,  UNIVERSITY  OF  CALIFORNIA,  DAVIS 

Book  Slip-35rn-7,'62(D296s4)458 


SPEEDY 

BINDER 

<*- 

Manufactured  by 

GAYUORDBROS.  Ine 

Syracuse,  N.Y. 

Stockton,  Calif. 


Q.L568 

A6 

•ps 


104189 


